Clemson University TigerPrints
All Dissertations Dissertations
May 2019 Enhancing Native Pollinators of Watermelon Agroecosystems in South Carolina Miriam Meryl Jenkins Clemson University, [email protected]
Follow this and additional works at: https://tigerprints.clemson.edu/all_dissertations
Recommended Citation Jenkins, Miriam Meryl, "Enhancing Native Pollinators of Watermelon Agroecosystems in South Carolina" (2019). All Dissertations. 2382. https://tigerprints.clemson.edu/all_dissertations/2382
This Dissertation is brought to you for free and open access by the Dissertations at TigerPrints. It has been accepted for inclusion in All Dissertations by an authorized administrator of TigerPrints. For more information, please contact [email protected]. ENHANCING NATIVE POLLINATORS OF WATERMELON AGROECOYSTEMS IN SOUTH CAROLINA
A Dissertation Presented to the Graduate School of Clemson University
In Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy Wildlife and Fisheries Biology
by Miriam Meryl Jenkins May 2019
Accepted by: Dr. Robert Baldwin, Committee Chair Dr. B. Merle Shepard Dr. Peter Adler Dr. William Bridges Dr. Amnon Levi ABSTRACT
Widespread declines in both managed and wild pollinators worldwide has led to
increasing concern for the valuable ecosystem services they provide for natural systems
and agriculture. This study examined the potential benefits of diversifying agricultural
landscapes by increasing floral diversity on farms on insect biodiversity and crop pollination services. My focal species, watermelon Citrullus lanatus, is an ideal species
for pollination studies because it is entirely dependent on insect pollinators to set fruit.
Chapter 1 investigates the effect that wildflower strips on watermelon farms has on the
delivery of pollination services to watermelon by the pollinator community. Chapter 2 presents information on the effects that wildflower strips on watermelon fields has on the biodiversity of the overall pollinator community. Chapter 3 examines the foraging behavior of several watermelon pollinator species to determine whether pollinator sharing
occurs between wildflower species and watermelon species when they occur
sympatrically. Chapter 4 is intended as an extension publication for the general public to
gain valuable information about wildflower strips on watermelon farms and the
conservation of native pollinators.
ii ACKNOWLEDGMENTS
Funding for this work was provided by the Agricultural Society of South
Carolina, The Watermelon Promotion Board, and the Margaret Lloyd Smartstate
Endowment.
Many volunteers provided invaluable hours of work on this project, along with generally making the experience more enjoyable. Thank you to Bailey Jones, Hannah
Mulligan, Kyle Russi, Abigail Rath, Kris Kuhn, Michael O’Cain, Grayson Vevon,
Catherine Eaves and Travis Cherry. Special thanks to my three diligent field assistants,
Kyle Baumis, Austin Weinheimer and Julianna Culbreath.
Sidi Limehouse at Rosebank Farm, the Freeman brothers at Freeman Farm, and
Bo Richardson at Dixie Farm provided sage advice and access to their farmland. Dr.
Shaker Kousik and Jennifer Ikerd at USDA Vegetable Laboratory provided supplies, advice, greenhouse space, and access to fields. Dr. Tony Keinath and Dr. Amnon Levi also provided access to fields at USDA and Clemson Coastal Research Center.
Sam Droege at USGS Native Bee Monitoring and Inventory Lab provided taxonomic identification, advice, and was kind enough to provide lodging for my visits.
Thank you to my committee for their input, especially Dr. Bridges for help with the statistical analysis. Elaine Sotherden also assisted with statistical analysis.
To my family and closest friends, thank you for your support and help throughout this process. And to my incredible husband, Nestor, thank you for wiping the tears off my face, keeping me company in the field on long days, and being the greatest gift in my life.
Te amo sapo.
iii TABLE OF CONTENTS
Page
TITLE PAGE ...... i
ABSTRACT ...... ii
ACKNOWLEDGMENTS ...... iii
LIST OF TABLES ...... vi
LIST OF FIGURES ...... viii
CHAPTER
I. WILDFLOWER STRIPS INCREASE WATERMELON VISITATION BY SELECT POLLINATORS...... 1
Abstract ...... 1 Introduction ...... 1 Materials and Methods ...... 4 Results ...... 9 Discussion ...... 13 Conclusion ...... 21 References ...... 22 Figures and Tables ...... 34
II. NATIVE POLLINATOR ASSEMBLAGE OF WATERMELON ON SOUTH CAROLINA FARMS ...... 44
Abstract ...... 44 Introduction ...... 44 Materials and Methods ...... 48 Results ...... 53 Discussion ...... 60 Conclusion ...... 72 References ...... 73 Figures and Tables ...... 90
III. FORAGING BEHAVIOR OF WATERMELON POLLINATORS ...... 112
iv Table of Contents (Continued)
Page
Abstract ...... 112 Introduction ...... 113 Materials and Methods ...... 119 Results ...... 121 Discussion ...... 123 Conclusion ...... 129 References ...... 130 Figures and Tables ...... 141
IV. PLANTING WILDFLOWER STRIPS ON WATERMELON FIELDS TO SUPPORT NATIVE POLLINATOR BIODIVERSITY ...... 144
Why conserve biodiversity of the pollinator community? ...... 144 Why include on-farm enhancements? ...... 150 How can I enhance native pollinators on farms? ...... 155 Could wildflowers draw pollinators away from my crop or have other negative consequences? ...... 161 What are the most common native pollinators on watermelon fields in South Carolina and how can I protect them? ...... 166
v LIST OF TABLES
Table Page
1.1 Effect of treatment, season, and treatment*season interaction on visitation frequency (mean number of visits per 45 second observation of 1m2 watermelon plots) of 6 pollinator groups and the sum of all visits on watermelon flowers in 2016-2018 ...... 35
1.2 Means and standard errors of visitation frequency of six pollinator groups and the sum of all visits by year and by treatment ...... 38
1.3 Means and standard errors of visitation frequency of six pollinator groups and sums of all visits by year and by season ...... 39
1.4 Means and standard errors of overall visitation frequency by year and by treatment in 2016-2018...... 40
1.5 Wildflower species in 2016 treatment fields ...... 43
2.1 Number of sampling events by site, year, specimens collected, and species richness (S)...... 90
2.2 Citrullus lanatus visitors by number of individuals collected per year, number of sites where they were collected/observed on C.lanatus, whether they were collected/observed on wildflower species ...... 91
2.3 List of wildflower visitors by number of sites where they were collected/ observed, total number of individuals collected over four years per floral species, whether they were also collected/observed on Citrullus lanatus and what bee guild they belong to if a bee ...... 96
2.4 Species and number of specimens collected with bee bowls in 2016...... 101
2.5 Jaccard similarity matrix of pollinator community composition for all fields by year ...... 102
2.6 Means and standard error of Jaccard similarity indices of pollinator community composition by year between watermelon fields with (treatment) and without (control) wildflowers in 2016 and 2017, and fields with wildflowers near the field and within the field in 2018 ...... 104
vi List of Tables (Continued)
Table Page
2.7 ANOVA test for difference between Jaccard similarity means in 2016 (control fields mean similarity index vs. treatment fields mean similarity index), 2017 (same as 2016), 2018 (wildflowers within fields mean similarity index vs. wildflowers near field mean similarity index)...... 105
2.8 Jaccard similarity of pollinator community composition between paired watermelon fields in 2017 ...... 106
2.9 Jaccard similarity of pollinator community composition for watermelon fields studied multiple years ...... 107
2.10 Wildflower species in 2016 treatment fields...... 111
3.1 Duration of visits per pollinator species on single watermelon flowers in South Carolina watermelon fields ...... 141
3.2 Floral constancy exhibited by bee pollinators of Citrullus lanatus on watermelon fields with co-flowering wildflowers and watermelon .... 143
vii LIST OF FIGURES
Figure Page
1.1 Proportion of visits to watermelon flowers by six pollinator groups...... 34
1.2 Mean visitation frequency per pollinator group on watermelon flowers in fields with and without wildflower treatments ...... 36
1.3 Mean visitation frequency per pollinator group on watermelon flowers in fields with wildflowers (WF) in the field vs. wildflowers near the field37
1.4 Proportions of visits by 6 pollinator groups to watermelon flowers by field type and year ...... 41
1.5 Correlation between mean density of watermelon flowers/m 2 per field and mean sums of total visits per field per day in 2016-2018 ...... 42
2.1 Number of pollinator species collected in 2015-2018 visiting focal species (Citrullus lanatus ) and wildflower species ...... 95
2.2 Total number of pollinator species including observed and collected species at control fields (grey) and treatment fields (black and white) in 2016 (A), 2017 (B) and 2018 (C) ...... 100
2.3 Species accumulation curve for all pollinator species using all sampling events (167) ...... 108
2.4 Individual rarefaction curve for 28 sites where pollinators were collected from watermelon fields for four years ...... 109
2.5 Individual rarefaction curves of all species collected in a) 2016 b) 2017 and c) 2018...... 110
3.1 Flower handling time in seconds per bee species on C. lanatus flowers ... 142
viii CHAPTER ONE
WILDFLOWER STRIPS INCREASE WATERMELON VISITATION BY SELECT POLLINATORS
Abstract – Agricultural intensification has negatively impacted biodiversity and ecosystem services supported by natural systems that contribute to agricultural productivity, including pollination services. One commonly recommended yet understudied method of diversifying farm landscapes is planting additional floral resources in wildflower strips or hedgerows. This extends the flowering period beyond the crop bloom and increases floral species richness to support native and managed pollinators. My study is the first to test the effect of wildflower strips on watermelon
(Citrullus lanatus ) pollination. I found that in each of three years (2016-2018), wild bees contributed the majority of visits to watermelon in 21 fields in South Carolina, especially the small sweat bee genus Lasioglossum spp. Wildflower strips significantly increased the watermelon visitation rate of Lasioglossum spp. but not of other pollinator groups.
Honey bees were significantly more frequent watermelon visitors in fields without wildflowers in one year, suggesting a potential lack of competition with native pollinators when additional resources and floral species richness are absent.
INTRODUCTION
To feed a growing human population, agricultural intensification is increasing globally, accounting for 80% of global deforestation and 70% of water withdrawals. It is also is the largest contributor to carbon emissions contributing to climate change (FAO,
2017). With this land use intensification comes degradation of agro-ecosystems, natural
1 habitats and the ecosystem services these areas provide (Tilman et al., 2001). This trend threatens biodiversity and the ecosystem services on which agriculture depends, including crop pollination (Garibaldi et al., 2011; Klein et al., 2007). Pollinator- dependent crops contribute to about 35% of global food production, and about 75% of leading food crops benefitting from animal pollinators in terms of yield or quality (Klein et al., 2007). The demand for pollinator-dependent crops is on the rise (Aizen et al., 2008;
Intergovernmental Science‐Policy Platform on Biodiversity and Ecosystem Services,
2016) while alarming rates of decline are being observed in both wild and managed pollinator populations (Intergovernmental Science‐Policy Platform on Biodiversity and
Ecosystem Services, 2016; Kluser and Peduzzi, 2007; Committee on the Status of
Pollinators in North America., 2007). The European honey bee ( Apis mellifera ) remains the most important managed agricultural tool for pollination, but is facing numerous threats including pests, disease, and insecticides resulting in average annual losses in the
US of 40-50% since 2006 (Lee et al., 2015). Wild pollinators are less studied but also are declining (Colla and Packer, 2008; Potts, S.G., Biesmeijer, J.C., Kremen, C., 2010;
Steffan-Dewenter et al., 2005). An estimated 40% of the world’s invertebrate pollinators are at risk of extinction (Intergovernmental Science‐Policy Platform on Biodiversity and
Ecosystem Services, 2016). A lack of sufficient floral and nesting resources, combined with insecticide use from agriculture and spread of pests and disease from managed species, are the most important factors in the decline of native bees (Apoidea), considered the most important pollinator group (Kearns et al., 1998; Kremen et al., 2002).
2 As more agricultural land is intensively managed, vast monocultures cover the landscape, limiting the availability of floral resources for pollinators beyond the relatively short period of crop bloom. The common practice of intense herbicide use along field edges and margins where weedy flowers could grow (Stoate et al., 2001) exacerbates the lack of floral and potential nesting resources. This lack of resource availability can reduce insect pollinator diversity and potentially decrease wild insect contributions to crop pollination (Potts et al., 2010). One commonly suggested method of improving conditions for pollinators in agro-landscapes is planting alternative floral resources, i.e. wildflower strips or hedgerows, to increase floral diversity, food resources and potential nesting sites (Carreck and Williams, 2002; Garibaldi et al., 2014; Heard et al., 2007;
Kremen et al., 2004). These additional food resources support native pollinator populations and biodiversity, which are critical to the stability, resilience and functionality of pollinator communities (Kremen et al., 2002; Mandelik et al., 2012), especially since bee populations are highly variable across space and time (Roubik, 2001;
Williams et al., 2001). The Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES) Report on Pollinators (2016) recommends “creating uncultivated patches of vegetation such as field margins with extended flowering periods” as one method to improve current conditions for pollinators. Farm bill conservation programs in the United States and agri-environmental schemes in the
European Union provide subsidies to incentivize farmers to plant additional floral resources on farms (Vaughan and Skinner, 2015). Some studies have found positive effects of wildflower plantings in agricultural fields by increasing the pollination
3 services, diversity and abundance of the native pollinator community in mango
(Carvalheiro et al., 2012), highbush blueberry (Blaauw and Isaacs, 2014), tomato (Balzan et al., 2016a), and strawberry (Feltham et al., 2015). Still, relatively little is known about the potential benefits of these widespread recommended techniques to individual flowering crop species, and the interactions with landscape context and farming management practices (Garibaldi et al., 2014; Kremen and M’gonigle, 2015).
My study species, watermelon ( Citrullus lanatus L.), is a monoecious crop entirely dependent on insect pollination to set fruit (Delaplane et al., 2000) Previous research has shown that native pollinators can provide all the pollination services to watermelon needed to produce marketable fruit if certain ecological conditions on the farm are met (Kremen et al., 2004; Winfree et al., 2008, 2007). My study is a response to repeated calls for more research on the potential impacts of additional floral resources on different crops (Sardiñas and Kremen, 2015; Winfree et al., 2008). It is the first study to investigate the impacts of wildflower strips on pollination services to watermelon. The overall objective of this research is to test the effectiveness of wildflower strips to improve pollination services to watermelon and to provide information that can be applied by farmers by (1) understanding the contribution of different insect pollinator groups to watermelon pollination on farms in coastal and central South Carolina, (2) determining the effect of wildflower patches on watermelon pollination services via visitation frequency, and (3) determining the effect of wildflower patches on the proportion of visits by different pollinator groups to watermelon pollination.
MATERIALS AND METHODS
4 Study species
Watermelon ( Citrullus lanatus L.) is a monoecious flowering crop and a low growing vine that prefers dry, sandy soil and high temperatures. Young seedlings were planted into the fields between March and May, with peak flowering occurring in June and July and a total flowering period of approximately two months. Watermelon flowers open one to two hours after sunrise, close between noon and 13:30 EDST depending on weather conditions, and do not reopen once closed (Mcgregor, 1976, M. Jenkins, personal observation). Staghellini (2002) found that 0600-1000 was the most important time for pollen deposition in producing fruit. Multiple varieties were planted in my study sites, including both triploid seedless SP7 and diploid seeded varieties Charleston Gray,
Sugar Baby and Crimson Sweet.
Study sites
The study was conducted in coastal and central South Carolina in Charleston,
Barnwell, and Bamburg Counties in the Southern Coastal Plain and Middle Atlantic
Coastal Plain ecoregions of the southeastern US. In 2016, six watermelon fields served as independent sites, at Clemson University Coastal Research Center in Charleston, South
Carolina, Clemson University Edisto Research Center in Blackville, SC and a commercial grower’s field in Olar, SC. The fields were separated by at least 500 m and ranged in size from 0.3 – 2 acres. Three fields were conventional monoculture watermelon fields and three fields were “diversified” fields, containing wildflowers and other co-flowering crop species intermixed with the watermelon crop. Wildflower plantings consisting of thirteen species of native wildflowers (Supplementary Info Table
5 1.5), which were transplanted into the three “diversified” watermelon fields in four 2m long sections within each row in spring 2016. The wildflowers flowered before, during, and after the watermelon flowering period. Fields adjacent to all study sites contained a range of crops consisting of tomatoes, corn, watermelon, squash, cantaloupe and cucumber but were separated from my fields by at least 100m.
In 2017, the study paired fields together in blocks to account for environmental heterogeneity in the landscape, climate, and other factors that could also influence pollinator communities and behavior. Five treatment fields were paired with five control fields in similar locations and with similar conditions in terms of chemical spraying, flowering period of watermelon, and field size. Six of these fields were at the Clemson
Coastal Research Center in Charleston SC, two fields at Clemson Edisto Research Center in Blackville, SC, and two at a small polyculture farm on John’s Island, SC. Each treatment field had one ~60m x 1m row of wildflowers on one edge of the field that flowered before, during, and after the watermelon flowering period. The wildflower strips consisted of 20 plots of four wildflower species transplanted as seedlings. Each of the four flower species comprised five 1m 2 plots with 20 plants per plot, separated by 1m between each plot. The wildflower seeds were not treated and were germinated from seed in February and March at the USDA Vegetable Laboratory in Charleston, SC in a greenhouse and outdoors. They were transplanted into each treatment field in April or
May 4-6 weeks before watermelons were transplanted into each field so that they would be flowering before watermelon. The four wildflower species, Yellow Zinnia (cardinal)
Zinnia elegans, Indian blanket Gaillardia pulchella, Plains Coreopsis Coreopsis tinctoria
6 and Sulphur Cosmos Cosmos sulphureus, were chosen based on drought tolerance, hardiness, length of flowering period, difference in flowering phenology, and previous observations in watermelon fields regarding their attraction to a wide diversity of pollinators. The 5 control watermelon fields did not contain wildflower strips.
In 2018, ten fields in Charleston and Barnwell Counties, SC were included in the study.
All fields this year contained wildflowers but differed in wildflower location; wildflowers were either in the field or near the field within 50-100m. Five fields were located on two small polyculture farms on John’s Island, SC, at Clemson Edisto Research Center in
Blackville, SC and Clemson Coastal Research Center in Charleston, SC with multiple crops present. Zinnia elegans, Verbena hastata, and Monarda fistulosa, made up the majority of the wildflower species near these fields. Three fields were also at the
Clemson Coastal Research and Education Center in Charleston SC and contained wildflower strips (G.pulchella, Z.elegans, C. tinctoria, C.sulphureus ) in a ~60m x 1m strip along one edge of each field, as was done in treatment fields in 2017. In 2016-2018, two to three honey bee hives were placed near all the fields. No commercial Bombus impatiens colonies were placed near the fields.
The density of watermelon flowers in each field was sampled to control for the effect that floral density may have on pollinator foraging behavior. In 2016-2018, 20 random 1m 2 plots were sampled for density of open watermelon flowers in each field one to four times throughout the flowering period of each field.
Pollinator observations
7 During 2016-2018, to determine the visitation frequency by different groups of pollinators, one to five people observed 1x1m 2 plots of watermelon flowers in each field from 0800-1200 EDST on mostly sunny days (<50% cloud cover). Observations were completed during the peak watermelon flowering period, which differed for each field, ranging from May 23-August 21. Observations were made along a 50m transect on a different row for each observer that traversed the length of each field, beginning always at the field edge. For a 45-second period, the observer(s) recorded the total number of insect visits to all watermelon flowers within a 1m2 plot in the watermelon row. A minimum of five watermelon flowers was required in each plot. The observer then moved
5 m along the transect and repeated the observation procedure for a new plot. In 2016,
20-60 plots were completed per observation period and in 2017 and 2018, 20 plots were completed per observation period, with multiple observation periods per day if weather permitted. Pollinators were separated into six distinguishable groups because it was not possible to identify to species or genus in the field. The groups were based mostly on size and general coloration pattern and consisted of large bees ( Bombus spp., Xylocopa spp.), medium bees ( Megachile spp., Melissodes spp., Halictus spp.), metallic green bees
(Agapostemon spp., Augochlorini), tiny bees ( Lasioglossum spp., Ceratina spp.), honey bees ( Apis mellifera ), and other insects (Lepidoptera, Diptera, other Hymenoptera).
Occasional Hemiptera were observed in flowers and were excluded because they were mostly predatory species (Reduviidae) with limited mobility and likely not transferring pollen. Spotted cucumber beetles Diabrotica undecimpunctata (Chrysomelidae) were also observed but were excluded because they are considered cucurbit pests and remained
8 on single flowers for long periods of time, making them unlikely pollinators for a monoecious plant.
Statistical analysis
To reduce zero counts and improve data normality, transects, observers and observation periods were pooled for individual days of observations for each site. The number of insects in each pollinator group was averaged across transects, then averaged across all observers in an observation period and finally across number of plots in a transect, generating a mean number of insects observed per pollinator group. Data from
2018 were square-root transformed to account for high variance and ensure data normality. Temporal differences within one field season were included as a variable by separating each season into early (May 15-June 15), middle (June 16-July 15), and late
(July 16-August 21). A separate ANOVA analysis for each year was conducted using standard least squares to test the effect of treatment, season, and treatment*season on the visitation rate of six pollinator groups and the sum of total insect visitation rate. All significance tests used an alpha of 0.05. Density of mean watermelon flowers per m 2 was correlated using linear regression between density of watermelon flowers and sums of total insect visits collected within seven days of when the density was sampled. All statistical calculations were performed using JMP (Version 8, SAS Institute Inc, Cary,
NC, USA).
RESULTS
In the summers of 2016-2018, a total of 6,279 observations of pollinators on 1m 2 plots were completed in 21 total watermelon fields. In 2016, pollinators were observed on
9 29 days from June 8-August 1, 2016, with 9,477 observations of watermelon-pollinating insects. In 2017, pollinators were observed on 40 days from June 14-August 21, 2017, with a total of 5,554 watermelon-pollinating insects. In 2018, pollinators were observed on 21 days from May 23-July 29, 2018, with 2,606 observations of watermelon- pollinating insects.
Visits from native bees made up the majority of total insect visitation of watermelon flowers. The most common were large bees (i.e. bumble bees (Bombus spp.) and large carpenter bees ( Xylocopa spp.)), medium bees (i.e. long-horned bees
(Melissodes spp.), leafcutter bees ( Megachile spp.) and Halictus spp.), and tiny bees (i.e.
Lasioglossum spp. and small carpenter bees ( Ceratina spp.)), comprising three families of bees (Apidae, Halictidae, Megachilidae). Honey bees were not the most frequent visitor in most fields despite hives being placed near all the fields specifically for watermelon pollination. Overall, in 2016-2018, four groups of native bees made up 64 - 76% of the total visits, honey bees 20 - 29%, and other insects 4 - 7%. In 2018, large bees made up
29.3% of the total visits, honey bees 26.3% of visits and tiny bees 23.8% of visits. The rest of the visits were made up of medium bees (9.7%), other insects (7.2%), and metallic green bees ( Agapostemon spp, Augochlorini; 3.7%). In 2017, tiny bees made up 34.3% of the total visits, followed by honey bees (28.6%), large bees (13.7%), medium sized bees
(13.7%), other insects (7%), and metallic green bees (2.5%) (Figure 1.1). This differed slightly from 2016 results, in which tiny bees and large bees made up almost equivalent proportions of the total number of visitations at all sites, with 25.8% and 25.0% of total visits, respectively. Medium-sized bees were the third most frequent visitors in 2016,
10 making up 21.9% of visits in 2016, followed by honey bees (19.7%), other insects (3.9%) and metallic green bees (3.5%) (Figure 1.1).
In 2016 and 2017, wildflower plantings had a significant positive effect on pollinator visitation frequency for the tiny bee group consisting mostly of the genus
Lasioglossum (F(1, 23)=10.78 , p=0.003 (2016), F(1,34)=7.78, p=0.009 (2017) Table
1.1). The tiny bee visitation rate was significantly higher in treatment fields (1.59 SE ±
0.30 (2016), 1.10 SE ± 0.24 (2017)) than in control fields (0.17 SE ± 0.08 (2016), 0.33
SE ± 0.06 (2017)) in both years (Table 1.2). In 2017 only, wildflower plantings had a significant positive effect on honey bee visitation rate (F(1, 34)= 8.21, p=0.007).
However, honey bee visitation was significantly higher in control fields (0.93 SE ± 0.21) than in treatment fields (0.58 SE ± 0.16). There was no significant effect of treatment on visitation frequency of large bees, medium bees, green bees, or other insect visitation frequency in 2016 and 2017 (Figure 1.2). In 2018, wildflower placement (within field versus near field) significantly affected large bee visitation rate (F(1,15)=5.48, p=0.03) but no other pollinator group (Table 1.1). Fields with wildflowers nearby had significantly higher large bee visitation (0.93 SE ± 0.21) compared to fields with wildflowers within the field (0.20 SE ± 0.12) (Table 1.2) (Figure 1.3).
Season was found to have a significant effect in 2017 on the total sum of all visits
(F(2,34)=21.03, p<.0001), green bee visitation (F(2,34)=10.53, p<0.001), tiny bee visitation (F(2,34)=3.69, p=0.04), honey bee visitation (F(2,34)=16.77, p<0.0001), and other insect visitation (F(2,34)=3.97, p=0.03) (Table 1.1). These visitation rates were all highest in the late season compared to the middle and early seasons (Table 1.3). There
11 was no significant effect of season on large and medium bee visitation rate in 2017, nor on any of the pollinator groups visitation rate in 2016 or 2018. The interaction effect had a significant positive effect for only honey bee visitation in 2017 (F(2,34)=5.91, p=0.006). No interaction effect was found for any pollinator group visitation in 2016 or
2018, except for the total visitation rate in 2018 indicating that the treatment effect for the total visitation rate in 2018 varied according to season (F (2,15)=4.20, p=0.04) (Table
1.1).
In 2016 and 2017, honey bees had the highest mean visitation frequency per 1m 2 plot in control fields (1.09 SE ± 0.32 (2016), 0.93 SE ± 0.21 (2017)) and tiny bees had the highest mean visitation frequency in treatment fields (1.59 SE ± 0.30 (2016), 1.10 SE
± 0.24 (2017)). In 2016, other insects had the lowest mean visitation frequency in control fields (0.09 SE ±0.02) and green bees were lowest in treatment fields (0.06 SE ±0.02)
(Table 1.2). In 2017, green bees had the lowest mean visitation frequency in both treatment and control fields (0.08 SE ± 0.03, 0.08 SE ± 0.03). In 2018, in fields with wildflowers within the field, tiny bees had the highest overall mean visitation frequency
(0.66 SE ± 0.20) and other insects had the lowest visitation frequency (0.11 SE ± 0.03).
In fields with wildflowers near the field, large bees had the highest visitation rate (0.93
SE ±0.21), and green bees had the lowest visitation rate (0.03 SE ± 0.01).
When visits were pooled by treatment type in each year, the pollinator community contained all of the six pollinator groups, with no single group dominating the total number of visits (Figure 1.4). Overall visitation rates by all species were lower in 2018
(2.02 SE ±0.21) than in the previous two years (3.11 SE ±0.24 in 2016, 2.45 SE ± 0.26 in
12 2017). Overall visitation rates by treatment were slightly higher in control fields (3.24 SE
± 0.45) than in treatment fields (3.03 SE ± 0.28) in 2016, but higher in treatment fields
(2.77 SE ± 0.39) than control fields (2.09 SE ± 0.32) in 2017. In 2018, near field visitation rates (2.31 SE ±0.29) were overall higher than within field (1.63 SE ±0.25)
(Table 1.4). Density of watermelon flowers in individual fields was not correlated with sums of total insect visits in 2016-2018 (R 2=0.000, y=2.607+0.007114x) (Figure 1.5).
DISCUSSION
Native bees provide important pollination services to watermelon crops in South
Carolina by contributing the majority of visits to C.lanatus flowers, with limited overall variability in their contribution over three years of study. Other insects such as wasps, flies and butterflies are much less frequent visitors to watermelon flowers, a trend in watermelon pollination studies (Kremen et al., 2004; Pisanty et al., 2016; Winfree et al.,
2008). Syrphid flies were by far the most common of the other insects that visit watermelon (M. Jenkins, personal observation). Despite growers and others placing honey bee hives near all fields to provide pollination services to the watermelon crop, they were not the most frequent visitors after calculating the mean visits from all fields.
However, fields varied considerably in terms of visitation rates by pollinator groups; some fields were visited evenly by all six pollinator groups, and some were dominated by two or three pollinator groups.
Previous studies have shown that many native bee species are more efficient pollinators of watermelon flowers because they deposit more pollen on watermelon stigmas per visit, tend to forage earlier in the morning when watermelon stigmas are
13 more receptive, and have a higher visitation rate due to faster foraging behavior than that of A. mellifera (Campbell et al., 2018; Kremen et al., 2002; Stanghellini et al., 2002) . For example, the common eastern bumble bee, Bombus impatiens, begins foraging 15 - 40 min earlier than A. mellifera , visits more watermelon flowers per minute and deposits more pollen, especially during the early hours of anthesis (Stanghellini et al., 2002).
Bombus impatiens deposits on average 369.8 (SE ± 68.3) pollen grains per visit on watermelon stigmas and Melissodes spp. deposits 338.6 (SE ± 38.1) grains, compared to
A. mellifera which deposits 177.4 (SE ± 31.5) grains per visit (Campbell et al., 2018). A minimum of 500 - 1000 pollen grains is required to successfully pollinate a watermelon flower, meaning six or more honey bee visits to set viable fruit versus two to three visits from a more effective forager such as Bombus spp. or Melissodes spp. (Adlerz, 1966;
Stanghellini, 1997). Therefore, it is especially important to support native bee populations for a crop like watermelon, which is more effectively pollinated by wild bees and might be more vulnerable to declines in honey bee visitation. In addition, behavioral, physiological and morphological differences in a diverse pollinator community lead to complementary resource use (niche complementarity) and enhanced pollination efficiency (Hoehn et al., 2008). Interspecific interactions between honey bees and wild bees can increase honey bee efficiency as honey bees are more likely to move more quickly and between rows when wild bees are present, resulting in higher fruit or seed set
(Brittain et al., 2013; Carvalheiro et al., 2011; Greenleaf and Kremen, 2006). If honey bee populations continue to decline and hive rental costs increase, native pollinators can buffer these losses and provide essential pollination services, given that management
14 efforts on farms allow them to persist. An estimated thirty million dollars per year could be redirected to conserving and restoring bee habitat if honey bee rentals by farmers were reduced by 15 - 50% (Kremen et al., 2002). An added incentive for farmers is that restoration costs can be partially covered for farmers and landowners by the Conservation
Reserve Program in the US and Agri-Environment Schemes in Europe (Kremen et al.
2002). Also Kremen et al. (2002) found that in California, about 50% of the wild bee species that visit watermelon visit other crops with equivalent or lower pollination requirements, so the bee community is likely providing pollination services for multiple crops, especially ones that honey bees cannot pollinate (i.e. cherry tomatoes). My results also show that in both treatment and control fields, the pollinator community was not dominated by one group of pollinators, indicating a diverse and sustainable source of pollination services to watermelon crop in my study area.
The most frequent pollinator of watermelon in my study was the tiny bee group, mostly consisting of Lasioglossum (Dialictus) spp., small ground-nesting halictid bees.
Lasioglossum (Dialictus) consists of small andreniform bees 3.4 - 8.1 mm long (Gibbs,
2011), well known for their diverse behaviors ranging from solitary (Packer, 1994), to communal (Eickwort, 1988), to semisocial (Sakagami et al., 1984), or eusocial (Batra,
1966; Eickwort, 1986). Colony sizes range from small (mean worker number less than 2
(Packer, 1992) to large (>100 workers, (Michener, 1966). This pollinator group was the only one in my study where we found significant differences in visitation rates in 2016 and 2017 between fields with wildflowers and control fields. Even with a relatively small area of floral diversity added to the farm landscape, the fields with wildflowers differed
15 in visitation rate by tiny bees of more than 9 times in 2016 and more than 3 times in
2017. Lasioglossum (Dialictus) were also the most frequent visitor of the six pollinator groups in fields with wildflowers in the field in 2018. Lasioglossum spp. tend to deposit lower levels of pollen per visit on watermelon stigmas (Kremen et al., 2002) with a mean of 138.7 (SE ± 33.8 grains) (Campbell et al., 2018). Other factors such as floral fidelity and foraging activity period contribute to foraging efficacy of pollinators, but floral visitation rates are the most important predictor of actual pollination (Vázquez et al.,
2005). Thus, since these bees had the highest visitation rate in treatment fields and foraged at earlier times in the morning, they might be important pollinators of watermelon despite their relatively low per-visit pollen deposition. Lasioglossum spp. are probably nesting in sandy, loamy soil near or within the field because their small size limits their foraging range (Gibbs, 2011; Greenleaf et al., 2007). Therefore, supporting their populations depends on tillage and spraying practices that limit soil disturbance.
Lasioglossum spp. frequently foraged on wildflowers ( Z.elegans, C.sulphureus,
C.tinctoria, G.pulchella ) planted in the treatment fields in 2016 and 2017 and within the fields in 2018, so they may benefit from higher floral diversity on agricultural fields (M.
Jenkins, personal observation). They might have had higher visitation when these wildflowers were in the fields in 2018 because of their small foraging range or they might be more attracted to the floral species in the field compared to ones nearby the field.
More research is needed on this speciose genus, of which there is still relatively little understood of the natural histories, which is necessary to develop management plans that can effectively protect them.
16 Honey bees had a significantly higher visitation rate in control fields than treatment fields in 2017 (and in 2016 but it was not statistically significant). This could be due to reduced competition with other native bees and insects that are drawn to an area and thus are more abundant when wildflowers are present. Alternatively, honey bees might have relied more on C. lanatus pollen and nectar when other floral resources were lacking nearby. Although honey bees were not commonly seen visiting wildflowers ( Z. elegans, G. pulchella, C. tinctoria, C. sulphureus ) in my treatment fields, they frequently visited “weedy” and cover crop flowers on roadsides and field edges near my treatment fields such as purple vetch ( Vicia americana ), wild mustard ( Sinapis sp.), verbena
(Verbena hastata ) and white and red clover ( Trifolium spp.) (M. Jenkins, personal observation). Efforts to support honey bees should include considerations of what floral species attract them. Additional floral resources in agricultural fields benefit honey bees because a more diverse source of nutrients and pollen improves the health and immune response of their brood (Alaux et al., 2010; Di Pasquale et al., 2013) and possibly decreases their risk of overexposure to pesticides commonly sprayed in agricultural fields.
In 2016 and 2017, the presence of wildflowers in watermelon fields affected visitation to watermelon flowers by just one pollinator group (tiny bees), while all other pollinator groups only saw small differences in visitation frequency between control and treatment fields. The overall visitation was slightly higher in control fields than in treatment fields in 2016; the opposite was seen in 2017, and visitation rates were higher in fields with wildflowers nearby than in fields with wildflowers in the field in 2018, but
17 not significantly different for any year. There could be multiple environmental effects unrelated to wildflower presence that made detecting any difference between my treatments challenging. The effects of additional resources provided by hedgerows and wildflower strips depend on crop identity and local landscape context (Sardiñas and
Kremen, 2015). The proportion of semi-natural habitat in an area can strongly influence the effect of additional floral resources and the extent to which pollinator communities rely on them. Thus, on-farm resources are likely more important and have a greater effect in agricultural areas with less semi-natural habitat nearby (Garratt et al., 2017; Tscharntke et al., 2005) The fields in my study were mostly in areas with high levels of habitat heterogeneity, consisting of small agricultural fields with weedy flowers growing along field edges, nearby roadsides and ditches. My study area in Charleston, South Carolina, and surrounding rural areas does not exhibit extreme agricultural intensity and most fields are within a few meters of pine forest, saltmarsh, or fallow fields. Thus, the diversified on-farm management and amount of semi-natural and natural areas surrounding farms in my study likely contribute to supporting a diverse pollinator community. High rates of human population increase in the Southeast and Charleston area specifically might change this with more intense land use and urbanization. In addition, the accessible flowers of C. lanatus attract a wide variety of generalists and specialists of different foraging ranges and habitat requirements, so the effects of wildflower strips in fields might not be as pronounced. Systems that more intensely rely on specialist pollinators may be more affected by additional resources depending on the nesting and food requirements and foraging ranges of the pollinator community.
18 In my 2018 study comparing visitation rates to C. lanatus between fields with wildflowers within the field versus near the field along the edges, large bees were the only pollinator group whose visitation rates were significantly different between field type, with higher visitation rates in fields with wildflowers nearby. This result implies that large bees are more apt to visit watermelon flowers when wildflowers are slightly further away from the crop flowers, along the field edges rather than intermixed in the field. These bee species could also be more drawn to the particular floral species on field edges instead of the wildflower species in the field. Xylocopa spp. and Bombus spp. in the large bee group can fly longer distances from their nests than smaller bees (Greenleaf et al., 2007), so they may detect floral resources at a larger spatial scale than can small solitary bees, that tend to nest near the preferred floral resource and not travel far in a foraging bout. One difficulty in detecting differences in visitation frequency might be due to the similarity between the fields with wildflowers nearby and in the field. The distance of the wildflowers from the crop row edge versus within the field may not have made a difference due to the mobility of all pollinators. Overall, the visitation rates to C. lanatus declined from 2016 to 2018 in my fields, which may be a point of concern for watermelon growers, although pollination environments are highly stochastic temporally and spatially. A three year assessment might not be sufficient to determine if a real decline is occurring (Roubik, 2001; Williams et al., 2001).
Wild bees also provided the majority of visits (62%) to watermelon in New Jersey and Pennsylvania across multiple land-use gradients (Winfree et al., 2008), providing sufficient pollination services at >90% of farms (Winfree et al., 2007). However, in
19 central California, honey bees were the dominant watermelon pollinator; wild bees contributed 34% of floral visits and were highly dependent on the proportion of natural upland habitat within 1.0 - 2.5 km of the farm (Kremen et al., 2004). Similarly, in central
Florida, honey bees were five times more abundant than were bumble bees in watermelon fields, which were not common even though B. impatiens colonies were stocked in the fields (Campbell et al., 2018). In central Israel, wild bees only accounted for 15% of visits and honey bees the remaining 85% even though most of the research fields did not have honey bees placed at the field (Pisanty et al., 2016). Benton et al. (2003) suggested that habitat heterogeneity is the key to restoring and maintaining biodiversity in temperate agricultural systems, and several studies find that distance to natural or semi- natural areas is an important predictor of crop pollination services (Blanche et al., 2006;
Klein, 2009; Kremen et al., 2004). The relatively low level of agricultural intensity in my area, smaller field sizes and floral species richness of crops and weedy flowers in surrounding fields might have led to the large contribution of wild bees to the pollination services in my study, similar to the results of Winfree et al. (2008). These small scale diversified agro-landscapes are globally threatened by agricultural intensification (Tilman et al., 2001), so this region should focus on limiting development or intensification of agriculture to ensure the future of local wild bee populations.
The lack of correlation between the density of the watermelon flowers and the total visitation rate is surprising, given that the opposite result is usually seen in plant- pollinator interaction studies. Higher plant density tends to correlate with higher floral visitation rate and higher floral constancy, leading to higher seed/fruit set (Kunin, 1993;
20 Steffan-Dewenter and Tscharntke, 2002). High floral species richness and close proximity to natural areas may limit this density-dependent effect on agricultural fields during the crop bloom period, especially if the crop flower is not as attractive as floral species in the surrounding land area.
Lastly, increasing floral diversity in the agro-landscape with wildflower strips and/or hedgerows has benefits beyond enabling pollinators to persist in the landscape and promoting crop pollination. These areas also provide habitat and food resources for beneficial insects such as predatory and parasitoid flies and wasps that control crop pests
(Balzan et al., 2016b; Ramsden et al., 2015), intrinsically valuable and rare or endangered species (Morandin and Kremen, 2013; Sardiñas and Kremen, 2015), and wildlife that rely on diverse insect communities as a food source (Staley et al., 2012). Supporting native pollinator populations also benefits wild plants and ecosystems since many crop pollinating species are generalists that pollinate many plant species, promoting conservation and biodiversity across agro-landscapes (Kremen et al., 2002). Measures to conserve wild pollinators will in turn conserve the regulating ecosystem services they provide which are critical to maintaining ecosystem function worldwide and conserving biodiversity and the intrinsic value of pollinators (Intergovernmental Science‐Policy
Platform on Biodiversity and Ecosystem Services, 2016; Kleijn et al., 2015).
CONCLUSION
Native pollinators play an important role in providing pollination services for a variety of crops and are keystone species in ecosystems worldwide (Garibaldi et al., 2013; Kleijn et al., 2015; Klein et al., 2007). Diversifying farms to support biodiversity is key to
21 reducing the impact that agricultural intensity has on ecosystems (Kennedy et al., 2013).
While agricultural landscapes can support abundant pollinator populations, the current declines in both honey bees and native bees display the negative impacts of habitat degradation and intense land use (Potts et al., 2010). For many crops, such as watermelon, the issue is compounded by their complete reliance on pollinators to produce fruit (Delaplane et al., 2000). My study is a response to the call for more science on native bees in agricultural systems, crop interactions and creating farm conditions that increase the abundance and diversity of wild pollinator populations. Planting wildflower strips to increase floral diversity and allowing weedy flowers to grow on field margins are two simple and inexpensive methods that farmers can implement and reap the benefits of a more stable, resilient, and sustainable pollinator community that does not rely on a single species.
REFERENCES
Adlerz, W.C., 1966. Honey Bee Visit Numbers and Watermelon Pollination. J. Econ.
Entomol. 59, 28–30. https://doi.org/10.1093/jee/59.1.28
Aizen, M.A., Garibaldi, L.A., Cunningham, S.A., Klein, A.M., 2008. Long-Term Global
Trends in Crop Yield and Production Reveal No Current Pollination Shortage but
Increasing Pollinator Dependency. Curr. Biol. 18, 1572–1575.
https://doi.org/10.1016/J.CUB.2008.08.066
Alaux, C., Ducloz, F., Crauser, D., Le Conte, Y., 2010. Diet effects on honeybee
immunocompetence. Biol. Lett. 6, 562–565. https://doi.org/10.1098/rsbl.2009.0986
22 Balzan, M. V., Bocci, G., Moonen, A.-C., 2016a. Utilisation of plant functional diversity
in wildflower strips for the delivery of multiple agroecosystem services. Entomol.
Exp. Appl. 158, 304–319. https://doi.org/10.1111/eea.12403
Balzan, M. V., Bocci, G., Moonen, A.-C., 2016b. Landscape complexity and field margin
vegetation diversity enhance natural enemies and reduce herbivory by Lepidoptera
pests on tomato crop. BioControl 61, 141–154. https://doi.org/10.1007/s10526-015-
9711-2
Batra, S., 1966. The Life Cycle and Behavior of the Primitively Social Bee,
Lasioglossum Zephyrum (Halictidae). Univ. Kansas Sci. Bull.
Benton, T.G., Vickery, J.A., Wilson, J.D., 2003. Farmland biodiversity: is habitat
heterogeneity the key? Trends Ecol. Evol. 18, 182–188.
https://doi.org/10.1016/S0169-5347(03)00011-9
Blaauw, B.R., Isaacs, R., 2014. Flower plantings increase wild bee abundance and the
pollination services provided to a pollination-dependent crop. J. Appl. Ecol. 51,
890–898. https://doi.org/10.1111/1365-2664.12257
Blanche, K.R., Ludwig, J.A., Cunningham, S.A., 2006. Proximity to rainforest enhances
pollination and fruit set in orchards. J. Appl. Ecol. 43, 1182–1187.
https://doi.org/10.1111/j.1365-2664.2006.01230.x
Brittain, C., Kremen, C., Klein, A.-M., 2013. Biodiversity buffers pollination from
changes in environmental conditions. Glob. Chang. Biol. 19, 540–547.
https://doi.org/10.1111/gcb.12043
Campbell, J.W., Daniels, J.C., Ellis, J.D., 2018. Fruit Set and Single Visit Stigma Pollen
23 Deposition by Managed Bumble Bees and Wild Bees in Citrullus lanatus
(Cucurbitales: Cucurbitaceae). J. Econ. Entomol. 111, 989–992.
https://doi.org/10.1093/jee/toy008
Carreck, N.L., Williams, I.H., 2002. Food for insect pollinators on farmland: insect visits
to flowers of annual seed mixtures. J. Insect Conserv. 6, 13–23.
https://doi.org/10.1023/A:1015764925536
Carvalheiro, L.G., Seymour, C.L., Nicolson, S.W., Veldtman, R., 2012. Creating patches
of native flowers facilitates crop pollination in large agricultural fields: mango as a
case study. J. Appl. Ecol. 49, 1373–1383. https://doi.org/10.1111/j.1365-
2664.2012.02217.x
Carvalheiro, L.G., Veldtman, R., Shenkute, A.G., Tesfay, G.B., Pirk, C.W.W.,
Donaldson, J.S., Nicolson, S.W., 2011. Natural and within-farmland biodiversity
enhances crop productivity. Ecol. Lett. 14, 251–259. https://doi.org/10.1111/j.1461-
0248.2010.01579.x
Colla, S.R., Packer, L., 2008. Evidence for decline in eastern North American
bumblebees (Hymenoptera: Apidae), with special focus on Bombus affinis Cresson.
Biodivers. Conserv. 17, 1379–1391. https://doi.org/10.1007/s10531-008-9340-5
Delaplane, K.S., Mayer, D.R., Mayer, D.F., 2000. Crop pollination by bees. CABI
Publishing.
Di Pasquale, G., Salignon, M., Le Conte, Y., Belzunces, L.P., Decourtye, A.,
Kretzschmar, A., Suchail, S., Brunet, J.-L., Alaux, C., 2013. Influence of Pollen
Nutrition on Honey Bee Health: Do Pollen Quality and Diversity Matter? PLoS One
24 8, e72016. https://doi.org/10.1371/journal.pone.0072016
Eickwort, G.C., 1988. Distribution patterns and biology of West Indian Sweat bees
(Hymenoptera: Halictidae).
Eickwort, G.C., 1986. First Steps into Eusociality: The Sweat Bee Dialictus lineatulus.
Florida Entomol. 69, 742. https://doi.org/10.2307/3495222
FAO, 2017. The future of food and agriculture – Trends and challenges. Rome, Italy.
Feltham, H., Park, K., Minderman, J., Goulson, D., 2015. Experimental evidence that
wildflower strips increase pollinator visits to crops. Ecol. Evol. 5, 3523–3530.
https://doi.org/10.1002/ece3.1444
Garibaldi, L.A., Aizen, M.A., Klein, A.M., Cunningham, S.A., Harder, L.D., 2011.
Global growth and stability of agricultural yield decrease with pollinator
dependence. Proc. Natl. Acad. Sci. U. S. A. 108, 5909–14.
https://doi.org/10.1073/pnas.1012431108
Garibaldi, L.A., Carvalheiro, L.G., Leonhardt, S.D., Aizen, M.A., Blaauw, B.R., Isaacs,
R., Kuhlmann, M., Kleijn, D., Klein, A.M., Kremen, C., Morandin, L., Scheper, J.,
Winfree, R., 2014. From research to action: enhancing crop yield through wild
pollinators. Front. Ecol. Environ. 12, 439–447. https://doi.org/10.1890/130330
Garibaldi, L.A., Steffan-Dewenter, I., Winfree, R., Aizen, M.A., Bommarco, R.,
Cunningham, S.A., Kremen, C., Carvalheiro, L.G., Harder, L.D., Afik, O.,
Bartomeus, I., Benjamin, F., Boreux, V., Cariveau, D., Chacoff, N.P., Dudenhöffer,
J.H., Freitas, B.M., Ghazoul, J., Greenleaf, S., Hipólito, J., Holzschuh, A., Howlett,
B., Isaacs, R., Javorek, S.K., Kennedy, C.M., Krewenka, K.M., Krishnan, S.,
25 Mandelik, Y., Mayfield, M.M., Motzke, I., Munyuli, T., Nault, B.A., Otieno, M.,
Petersen, J., Pisanty, G., Potts, S.G., Rader, R., Ricketts, T.H., Rundlöf, M.,
Seymour, C.L., Schüepp, C., Szentgyörgyi, H., Taki, H., Tscharntke, T., Vergara,
C.H., Viana, B.F., Wanger, T.C., Westphal, C., Williams, N., Klein, A.M., 2013.
Wild pollinators enhance fruit set of crops regardless of honey bee abundance.
Science 339, 1608–11. https://doi.org/10.1126/science.1230200
Garratt, M.P.D., Senapathi, D., Coston, D.J., Mortimer, S.R., Potts, S.G., 2017. The
benefits of hedgerows for pollinators and natural enemies depends on hedge quality
and landscape context. Agric. Ecosyst. Environ. 247, 363–370.
https://doi.org/10.1016/J.AGEE.2017.06.048
Gibbs, J., 2011. Revision of the metallic Lasioglossum (Dialictus) of eastern North
America (Hymenoptera: Halictidae: Halictini)Revision of the metallic Lasioglossum
(Dialictus) of eastern North America (Hymenoptera: Halictidae: Halictini). Zootaxa
3073, 1–216.
Greenleaf, S.S., Kremen, C., 2006. Wild bees enhance honey bees’ pollination of hybrid
sunflower. Proc. Natl. Acad. Sci. U. S. A. 103, 13890–5.
https://doi.org/10.1073/pnas.0600929103
Greenleaf, S.S., Williams, N.M., Winfree, R., Kremen, C., 2007. Bee foraging ranges and
their relationship to body size. Oecologia 153, 589–596.
https://doi.org/10.1007/s00442-007-0752-9
Heard, M.., Carvell, C., Carreck, N.., Rothery, P., Osborne, J.., Bourke, A.F.., 2007.
Landscape context not patch size determines bumble-bee density on flower mixtures
26 sown for agri-environment schemes. Biol. Lett. 3, 638–641.
https://doi.org/10.1098/rsbl.2007.0425
Hoehn, P., Tscharntke, T., Tylianakis, J.M., Steffan-Dewenter, I., 2008. Functional group
diversity of bee pollinators increases crop yield. Proc. R. Soc. B Biol. Sci. 275,
2283–2291. https://doi.org/10.1098/rspb.2008.0405
Intergovernmental Science‐Policy Platform on Biodiversity and Ecosystem Services,
2016. Summary for policymakers of the assessment report of the Intergovernmental
Science‐Policy Platform on Biodiversity and Ecosystem Services on pollinators,
pollination and food production. Bonn, Germany.
Kearns, C.A., Inouye, D.W., Waser, N.M., 1998. Endangered Mutualisms: The
Conservation of Plant-Pollinator Interactions. Annu. Rev. Ecol. Syst. 29, 83–112.
https://doi.org/10.1146/annurev.ecolsys.29.1.83
Kennedy, C.M., Lonsdorf, E., Neel, M.C., Williams, N.M., Ricketts, T.H., Winfree, R.,
Bommarco, R., Brittain, C., Burley, A.L., Cariveau, D., Carvalheiro, L.G., Chacoff,
N.P., Cunningham, S.A., Danforth, B.N., Dudenhöffer, J.-H., Elle, E., Gaines, H.R.,
Garibaldi, L.A., Gratton, C., Holzschuh, A., Isaacs, R., Javorek, S.K., Jha, S., Klein,
A.M., Krewenka, K., Mandelik, Y., Mayfield, M.M., Morandin, L., Neame, L.A.,
Otieno, M., Park, M., Potts, S.G., Rundlöf, M., Saez, A., Steffan-Dewenter, I., Taki,
H., Viana, B.F., Westphal, C., Wilson, J.K., Greenleaf, S.S., Kremen, C., 2013. A
global quantitative synthesis of local and landscape effects on wild bee pollinators in
agroecosystems. Ecol. Lett. 16, 584–599. https://doi.org/10.1111/ele.12082
Kleijn, D., Winfree, R., Bartomeus, I., Carvalheiro, L.G., Henry, M., Isaacs, R., Klein,
27 A.-M., Kremen, C., M’Gonigle, L.K., Rader, R., Ricketts, T.H., Williams, N.M.,
Lee Adamson, N., Ascher, J.S., Báldi, A., Batáry, P., Benjamin, F., Biesmeijer, J.C.,
Blitzer, E.J., Bommarco, R., Brand, M.R., Bretagnolle, V., Button, L., Cariveau,
D.P., Chifflet, R., Colville, J.F., Danforth, B.N., Elle, E., Garratt, M.P.D., Herzog,
F., Holzschuh, A., Howlett, B.G., Jauker, F., Jha, S., Knop, E., Krewenka, K.M., Le
Féon, V., Mandelik, Y., May, E.A., Park, M.G., Pisanty, G., Reemer, M., Riedinger,
V., Rollin, O., Rundlöf, M., Sardiñas, H.S., Scheper, J., Sciligo, A.R., Smith, H.G.,
Steffan-Dewenter, I., Thorp, R., Tscharntke, T., Verhulst, J., Viana, B.F., Vaissière,
B.E., Veldtman, R., Ward, K.L., Westphal, C., Potts, S.G., 2015. Delivery of crop
pollination services is an insufficient argument for wild pollinator conservation. Nat.
Commun. 6, 7414. https://doi.org/10.1038/ncomms8414
Klein, A.-M., 2009. Nearby rainforest promotes coffee pollination by increasing spatio-
temporal stability in bee species richness. For. Ecol. Manage. 258, 1838–1845.
https://doi.org/10.1016/J.FORECO.2009.05.005
Klein, A.-M., Vaissière, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A.,
Kremen, C., Tscharntke, T., 2007. Importance of pollinators in changing landscapes
for world crops. Proc. R. Soc. B Biol. Sci. 274, 303–313.
https://doi.org/10.1098/rspb.2006.3721
Kluser, S., Peduzzi, P., 2007. Global pollinator decline: a literature review.
Kremen, C., M’gonigle, L.K., 2015. Small-scale restoration in intensive agricultural
landscapes supports more specialized and less mobile pollinator species. J. Appl.
Ecol. 52, 602–610. https://doi.org/10.1111/1365-2664.12418
28 Kremen, C., Williams, N.M., Bugg, R.L., Fay, J.P., Thorp, R.W., 2004. The area
requirements of an ecosystem service: crop pollination by native bee communities in
California. Ecol. Lett. 7, 1109–1119. https://doi.org/10.1111/j.1461-
0248.2004.00662.x
Kremen, C., Williams, N.M., Thorp, R.W., 2002. Crop pollination from native bees at
risk from agricultural intensification. Proc. Natl. Acad. Sci. 99, 16812–16816.
https://doi.org/10.1073/pnas.262413599
Kunin, W.E., 1993. Sex and the Single Mustard: Population Density and Pollinator
Behavior Effects on Seed-Set. Ecology 74, 2145–2160.
https://doi.org/10.2307/1940859
Lee, K. V., Steinhauer, N., Rennich, K., Wilson, M.E., Tarpy, D.R., Caron, D.M., Rose,
R., Delaplane, K.S., Baylis, K., Lengerich, E.J., Pettis, J., Skinner, J.A., Wilkes, J.T.,
Sagili, R., vanEngelsdorp, D., Partnership, for the B.I., 2015. A national survey of
managed honey bee 2013–2014 annual colony losses in the USA. Apidologie 46,
292–305. https://doi.org/10.1007/s13592-015-0356-z
Mandelik, Y., Winfree, R., Neeson, T., Kremen, C., 2012. Complementary habitat use by
wild bees in agro-natural landscapes. Ecol. Appl. 22, 1535–1546.
https://doi.org/10.1890/11-1299.1
Mcgregor, S.E., 1976. Insect Pollination Of Cultivated Crop Plants.
Michener, C.D., 1966. The Bionomics of a Primitively Social Bee, Lasioglossum
versatum (Hymenoptera: Halictidae). J. Kansas Entomol. Soc.
https://doi.org/10.2307/25083507
29 Morandin, L.A., Kremen, C., 2013. Hedgerow restoration promotes pollinator
populations and exports native bees to adjacent fields. Ecol. Appl. 23, 829–839.
https://doi.org/10.1890/12-1051.1
National Research Council (U.S.). Committee on the Status of Pollinators in North
America., 2007. Status of pollinators in North America. National Academies Press.
Packer, L., 1994. Lasioglossum (Dialictus) tenax (Sandhouse) (Hymenoptera: Halictidae)
as a solitary sweat bee. Insectes Soc. 41, 309–313.
https://doi.org/10.1007/BF01242302
Packer, L., 1992. The social organisation of Lasioglossum (Dialictus) laevissimum
(Smith) in southern Alberta. Can. J. Zool. 70, 1767–1774.
https://doi.org/10.1139/z92-244
Pisanty, G., Afik, O., Wajnberg, E., Mandelik, Y., 2016. Watermelon pollinators exhibit
complementarity in both visitation rate and single-visit pollination efficiency. J.
Appl. Ecol. 53, 360–370. https://doi.org/10.1111/1365-2664.12574
Potts, S.G., Biesmeijer, J.C., Kremen, C., N., 2010. Global pollinator declines: trends,
impacts and drivers. Trends Ecol. Evol.
Ramsden, M.W., Menéndez, R., Leather, S.R., Wäckers, F., 2015. Optimizing field
margins for biocontrol services: The relative role of aphid abundance, annual floral
resources, and overwinter habitat in enhancing aphid natural enemies. Agric.
Ecosyst. Environ. 199, 94–104. https://doi.org/10.1016/J.AGEE.2014.08.024
Roubik, D., 2001. Ups and downs in pollinator populations:when is there a decline?
Conserv. Ecol. 5. https://doi.org/10.1234/2013/999990.
30 Sakagami, S.F., Hoshikawa, K., Fukuda, H., 1984. Overwintering ecology of two social
halictine bees, Lasioglossum duplex and L. problematicum. Res. Popul. Ecol.
(Kyoto). 26, 363–378. https://doi.org/10.1007/BF02515500
Sardiñas, H.S., Kremen, C., 2015. Pollination services from field-scale agricultural
diversification may be context-dependent. Agric. Ecosyst. Environ. 207, 17–25.
https://doi.org/10.1016/J.AGEE.2015.03.020
Staley, J.T., Sparks, T.H., Croxton, P.J., Baldock, K.C.R., Heard, M.S., Hulmes, S.,
Hulmes, L., Peyton, J., Amy, S.R., Pywell, R.F., 2012. Long-term effects of
hedgerow management policies on resource provision for wildlife. Biol. Conserv.
145, 24–29. https://doi.org/10.1016/J.BIOCON.2011.09.006
Stanghellini, M.S., 1997. The effects of honey bee and bumble bee pollination of fruit set
and abortion of cucumber and watermelon. Am. Bee J. 137, 386–391.
Stanghellini, M.S., Ambrose, J.T., Schultheis, J.R., 2002. Diurnal activity, floral
visitation and pollen deposition by honey bees and bumble bees on field-grown
cucumber and watermelon. J. Apic. Res. 41, 27–34.
https://doi.org/10.1080/00218839.2002.11101065
Steffan-Dewenter, I., Potts, S.G., Packer, L., 2005. Pollinator diversity and crop
pollination services are at risk. Trends Ecol. Evol. 20, 651-2; author reply 652-3.
https://doi.org/10.1016/j.tree.2005.09.004
Steffan-Dewenter, I., Tscharntke, T., 2002. Insect communities and biotic interactions on
fragmented calcareous grasslands—a mini review. Biol. Conserv. 104, 275–284.
https://doi.org/10.1016/S0006-3207(01)00192-6
31 Stoate, C., Boatman, N.., Borralho, R.., Carvalho, C.R., Snoo, G.R. d., Eden, P., 2001.
Ecological impacts of arable intensification in Europe. J. Environ. Manage. 63, 337–
365. https://doi.org/10.1006/JEMA.2001.0473
Tilman, D., Fargione, J., Wolff, B., D’Antonio, C., Dobson, A., Howarth, R., Schindler,
D., Schlesinger, W.H., Simberloff, D., Swackhamer, D., 2001. Forecasting
agriculturally driven global environmental change. Science 292, 281–4.
https://doi.org/10.1126/science.1057544
Tscharntke, T., Klein, A.M., Kruess, A., Steffan-Dewenter, I., Thies, C., 2005. Landscape
perspectives on agricultural intensification and biodiversity – ecosystem service
management. Ecol. Lett. 8, 857–874. https://doi.org/10.1111/j.1461-
0248.2005.00782.x
Vaughan M, Skinner M, 2015. Using 2014 Farm Bill Programs for Pollinator
Conservation. Biology Technical Note No. 78, 2nd ed.
Vázquez, D.P., Morris, W.F., Jordano, P., 2005. Interaction frequency as a surrogate for
the total effect of animal mutualists on plants. Ecol. Lett. 8, 1088–1094.
https://doi.org/10.1111/j.1461-0248.2005.00810.x
Williams, N.M., Minckley, R.L., Silveira, F.A., 2001. Variation in native bee faunas and
its implications for detecting community changes. Conserv. Ecol. 5.
Winfree, R., Williams, N.M., Dushoff, J., Kremen, C., 2007. Native bees provide
insurance against ongoing honey bee losses. Ecol. Lett. 10, 1105–1113.
https://doi.org/10.1111/j.1461-0248.2007.01110.x
Winfree, R., Williams, N.M., Gaines, H., Ascher, J.S., Kremen, C., 2008. Wild bee
32 pollinators provide the majority of crop visitation across land-use gradients in New
Jersey and Pennsylvania, USA. J. Appl. Ecol. 45, 793–802. https://doi.org/10.1111/j.1365-2664.2007.01418.x
33 2016 Other insects Honey 4% Large bees Bees 20% 25%
Tiny bees Medium Green Bees 26% Bees 3% 22%
2017 Other Large insects Bees 7% 14%
Honey Medium bees Bees 29% 14% Green bees 2%
Tiny bees 34%
2018 Other insects Large 7% bees Honey 29% bees 26%
Medium Green Bees Tiny bees bees 10% 24% 4%
Figure 1.1 Proportion of visits to watermelon flowers by six pollinator groups. Large bees consisted of Bombus spp. and Xylocopa spp., medium bees included Melissodes spp., Halictus spp., and Megachile spp., green bees included Agapostemon spp. and bees in the Augochlorini tribe, tiny bees included Lasioglossum spp., Ceratina spp., honey bees ( Apis mellifera), and other insects included Lepidopterans, Dipterans, and other Hymenopterans (occasional Hemipterans were observed in flowers and were excluded because they were mostly predatory species; occasional Diabrotica undecimpunctata (Chrysomelidae) were also observed but were excluded because they are considered cucurbit pests).
34 Table 1.1 Effect of treatment, season, and treatment*season interaction on visitation frequency (mean number of visits per 45 second observation of 1m 2 watermelon plots) of 6 pollinator groups and the sum of all visits on watermelon flowers in 2016-2018.
2016 Treatment Season Treatment*Season df F p df F p df F p total all groups 1,23 0.12 0.74 2,23 0.95 0.40 2,23 2.50 0.10 Large Bees 1,23 2.67 0.11 2,23 1.69 0.21 2,23 0.43 0.65 Medium Bees 1,23 0.76 0.39 2,23 0.23 0.79 2,23 0.58 0.56 Green Bees 1,23 0.09 0.76 2,23 0.39 0.68 2,23 1.03 0.37 Tiny Bees 1,23 10.78 0.003* 2,23 1.38 0.27 2,23 0.86 0.44 Honey Bees 1,23 2.63 0.12 2,23 0.82 0.45 2,23 1.68 0.21 Others 1,23 0.37 0.55 2,23 2.03 0.15 2,23 1.20 0.32
2017 Treatment Season Treatment*Season df F p df F p df F p total all groups 1,34 0.83 0.37 2,34 21.03 <.0001 2,34 0.40 0.67 Large Bees 1,34 0.00 0.98 2,34 2.86 0.07 2,34 0.20 0.82 Medium Bees 1,34 2.5 0.12 2,34 0.07 0.93 2,34 1.05 0.36 Green Bees 1,34 0.21 0.65 2,34 10.53 <.001* 2,34 0.014 0.87 Tiny Bees 1,34 7.78 0.009* 2,34 3.69 0.04* 2,34 1.62 0.21 Honey Bees 1,34 8.21 0.007* 2,34 16.77 <.0001*2,34 5.91 0.006* Others 1,34 0.00 0.97 2,34 3.97 0.03* 2,34 1.64 0.21
2018 Treatment Season Treatment*Season df F p df F p df F p total all groups 1,15 3.76 0.07 2,15 0.24 0.79 2,15 4.20 0.04* Large Bees 1,15 5.48 0.03* 2,15 0.28 0.76 2,15 0.57 0.57 Medium Bees 1,15 2.46 0.14 2,15 0.86 0.44 2,15 0.25 0.78 Green Bees 1,15 3.45 0.08 2,15 0.35 0.71 2,15 1.58 0.24 Tiny Bees 1,15 1.13 0.30 2,15 0.16 0.85 2,15 0.97 0.40 Honey Bees 1,15 0.63 0.44 2,15 0.15 0.86 2,15 1.24 0.32 Others 1,15 0.01 0.94 2,15 0.17 0.85 2,15 0.56 0.58
35 2016 2017
p<.01
2017 p<.01
Figure 1.2 Mean visitation frequency per pollinator group on watermelon flowers in fields with and without wildflower treatments. Large bees consisted of Bombus spp. and Xylocopa spp., medium bees included Melissodes spp., Halictus spp., and Megachile spp., green bees included Agapostemon spp. and bees in the Augochlorini tribe, tiny bees included Lasioglossum spp., Ceratina spp., honey bees ( Apis mellifera), and other insects included Lepidopterans, Dipterans, and other Hymenopterans. Error bars are 1 standard error from the mean. Tiny bees were significantly higher in treatment fields than in control fields in both 2016 (F(1, 23)=10.78 , p=0.003) and 2017 (F(1,34)=7.78, p=0.009). Honey bees were significantly higher in control fields than in treatment fields in 2017 (F(1, 34)= 8.21, p=0.007). No significant differences were found for the other pollinator groups between control and treatment field visitation frequency.
36 p=0.03
Figure 1.3 Mean visitation frequency per pollinator group on watermelon flowers in fields with wildflowers (WF) in the field vs. wildflowers near the field in 2018. Large bees consisted of Bombus spp. and Xylocopa spp., medium bees included Melissodes spp., Halictus spp., and Megachile spp., green bees included Agapostemon spp. and bees in the Augochlorini tribe, tiny bees included Lasioglossum spp., Ceratina spp., honey bees ( Apis mellifera), and other insects included Lepidopterans, Dipterans, and other Hymenopterans. Error bars are 1 standard error from the mean. Large bees were the only group that differed significantly in visitation frequency between the two field types (F(1,15)=5.48, p=0.03), with higher visitation in fields with wildflowers nearby.
37 Table 1.2 Means and standard errors of visitation frequency of six pollinator groups and the sum of all visits by year and by treatment (control/no wildflowers=C, treatment/wildflowers=T, within=wildflowers within field, near=wildflowers near field). Large bees consisted of Bombus spp. and Xylocopa spp., medium bees included Melissodes spp., Halictus spp., and Megachile spp., green bees included Agapostemon spp. and bees in the Augochlorini tribe, tiny bees included Lasioglossum spp., Ceratina spp., honey bees ( Apis mellifera), and other insects included Lepidopterans, Dipterans, and other Hymenopterans.
2016 2017 2018
Mean SE T/C Mean SE T/C Mean SE T/C
Total Sum 3.24 0.45 C 2.09 0.32 C 1.62 0.25 Within
3.03 0.28 T 2.78 0.39 T 2.31 0.29 Near
Large Bees 0.90 0.24 C 0.35 0.10 C 0.20 0.12 Within
0.43 0.05 T 0.41 0.10 T 0.93 0.21 Near
Medium Bees 0.85 0.34 C 0.24 0.07 C 0.14 0.07 Within
0.54 0.14 T 0.44 0.11 T 0.26 0.07 Near
Green Bees 0.13 0.07 C 0.08 0.03 C 0.18 0.06 Within
0.06 0.02 T 0.08 0.03 T 0.03 0.01 Near
Tiny Bees 0.17 0.08 C 0.33 0.06 C 0.66 0.2 Within
1.59 0.30 T 1.10 0.24 T 0.39 0.14 Near
Honey Bees 1.09 0.32 C 0.93 0.21 C 0.33 0.21 Within
0.26 0.11 T 0.58 0.16 T 0.55 0.18 Near
Others 0.09 0.02 C 0.16 0.04 C 0.11 0.03 Within
0.15 0.02 T 0.18 0.03 T 0.15 0.04 Near
38 Table 1.3. Means and standard errors of visitation frequency of six pollinator groups and sums of all visits by year and by season (early=May 15-June 15, mid=June 16-July 15, late=July 16-Aug 21). Large=large bees i.e. Bombus spp. and Xylocopa spp., Med=medium bees i.e. Melissodes spp., Halictus spp., and Megachile spp., Green=green bees i.e. Agapostemon spp. and bees in the Augochlorini tribe; Tiny=tiny bees i.e. Lasioglossum spp., Ceratina spp.; Honey=honey bees ( Apis mellifera); Others=other insects i.e. Lepidopterans, Dipterans, and other Hymenopterans.
2016 2017 2018
Early Mid Late Early Mid Late Early Mid Late
Mean SE Mean SE Mean SE Mean SE Mean SE Mean SE Mean SE Mean SE Mean SE
Total 3.51 0.66 3.29 0.27 2.63 0.23 1.30 0.17 1.87 0.32 4.14 0.34 2.24 0.49 1.92 0.34 1.89 0.24
Large 0.50 0.16 0.96 0.26 0.40 0.07 0.19 0.12 0.34 0.12 0.59 0.08 0.78 0.34 0.82 0.24 0.25 0.14
Med 0.93 0.42 0.66 0.24 0.44 0.13 0.32 0.10 0.32 0.12 0.40 0.13 0.16 0.11 0.24 0.06 0.24 0.10
Green 0.10 0.05 0.13 0.09 0.04 0.02 0.05 0.03 0.01 0.00 0.19 0.04 0.03 0.02 0.04 0.02 0.21 0.08
Tiny 1.26 0.63 0.58 0.23 1.27 0.23 0.28 0.10 0.59 0.16 1.27 0.34 0.51 0.17 0.31 0.15 0.71 0.27
Honey 0.63 0.29 0.85 0.35 0.31 0.18 0.31 0.10 0.50 0.18 1.42 0.24 0.65 0.28 0.32 0.16 0.40 0.26
Others 0.08 0.02 0.11 0.03 0.17 0.02 0.14 0.03 0.13 0.03 0.26 0.06 0.11 0.04 0.19 0.07 0.09 0.02
39 Table 1.4 Means and standard errors of overall visitation frequency by year and by treatment in 2016-2018.
Mean SE n Treatment Year
3.24 0.45 3 Control 2016 3.03 0.28 3 Treatment 2016 2.09 0.32 5 Control 2017 2.77 0.39 5 Treatment 2017 1.63 0.25 3 Within Field 2018 2.31 0.29 5 Near field 2018
Mean Overall Visitation Rate SE n Year
3.11 0.24 6 2016 2.45 0.26 10 2017 2.02 0.21 10 2018
40 Large Bees Medium Bees Green Bees Tiny Bees Honey Bees Others
Figure 1.4 Proportions of visits by 6 pollinator groups to watermelon flowers by field type and year. Large bees consisted of Bombus spp. and Xylocopa spp., medium bees included Melissodes spp., Halictus spp., and Megachile spp., green bees included Agapostemon spp. and bees in the Augochlorini tribe, tiny bees included Lasioglossum spp., Ceratina spp., honey bees ( Apis mellifera), and other insects included Lepidopterans, Dipterans, and other Hymenopterans.
41 A
B
Figure 1.5 Correlation between mean density of watermelon flowers/m 2 per field and mean sums of total visits per field per day in 2016-2018. A. Colored dots represent different field sites B. Colored dots represent treatment (C=control, T=treatment, WITHIN=wildflowers within the field, NEAR=wildflowers near the field). R 2=0.000, y=2.607+0.007114x
42
Supplementary information
Table 1.5 Wildflower species in 2016 treatment fields.
1. Scarlet Flax – Linum grandiflorum rubrum 2. Catch Fly – Silene armerla 3. Annual Baby’s Breath – Gypsophila elegans 4. Cornflower (Bachelor’s button) – Centaurea cyanus 5. Annual Gaillardia (Indian blanket) – Gaillardia pulchellia 6. Bachelor’s Button Tall mixed/Cornflower – Centaurea cynnus – Tall mixed 7. Cosmos – Cosmos bipinnatus 8. Sulphur Cosmos – Cosmos sulphureus 9. Plains Coreopsis – Coreopsis tinctoria 10. Sweet Alyssum – Lobularia maritima 11. Black eyed Susan, coastal plain NC Ecotype. Rudbeckia hirta 12. Spurred Snapdragon (Northern Lights) – Linaria maroccana 13. Annual Phlox – Phlox drummondii
43 CHAPTER TWO
NATIVE POLLINATOR ASSEMBLAGE OF WATERMELON ON SOUTH CAROLINA FARMS
Abstract -Agricultural landscapes can be attractive to pollinator species during periods of crop bloom, but a lack of floral resources beyond the crop flowering period, diminished natural areas nearby, an increase in the use of chemicals to control pests and disease, and frequent soil disturbance makes current agricultural systems unfavorable for many pollinator species. From 2016-2018, I investigated whether diversifying watermelon fields by transplanting wildflowers and retaining weedy flowers on field edges affected the species richness of wild pollinators. I found a higher species richness of wild pollinators in fields with higher floral diversity in both the watermelon and wildflower pollinator assemblages. I collected 59 species of native pollinators that visited watermelon flowers in 21 fields in central and coastal South Carolina . The number of bee species collected per year visiting C. lanatus was similar across years—with 35, 34 and
33 species collected in 2018, 2017 and 2016 respectively. Nomada vegana, a small cleptoparasitic bee, is a new state record for South Carolina. Most of these species were social ground nesting bees, but solitary ground nesting bees, cavity nesting bees, cleptoparasites, and bumble bees as well as syrphid flies, butterflies and wasps were collected visiting watermelon flowers and wildflowers. This study supports the management practice of planting wildflowers or hedgerows on farms to support a diverse community of wild pollinators for their pollination services and their role in natural ecosystems.
INTRODUCTION
44 Global declines in biodiversity have led to the 6 th mass extinction event on earth, threatening ecosystems, species persistence and ecosystem services (Butchart et al.,
2010). Pollinator populations have been sharply declining in the past 50 years, due to a combination of stressors including parasites, habitat destruction, lack of floral resources, and pesticide use (Goulson et al., 2015; National Research Council (U.S.), 2007). The
European honey bee Apis mellifera remains the most important managed agricultural tool for pollination, but is also facing multiple threats resulting in average annual losses in the
US around 40 - 50% since 2006 (Lee et al., 2015).
Wild pollinators are less understood but the most well-studied group, bumble bees, are exhibiting significant declines and range reductions (Colla and Packer, 2008;
Goulson et al., 2008; Potts et al., 2010; Steffan-Dewenter et al., 2005; Williams and
Osborne, 2009). The Intergovernmental Science-Policy Platform on Biodiversity and
Ecosystem Services estimated that 40% of the world’s invertebrate pollinators are at risk of extinction (Intergovernmental Science‐Policy Platform on Biodiversity and
Ecosystem Services, 2016), but little to no information exists about many wild species
(Goulson et al., 2015). Conserving the global biodiversity of pollinators is increasingly important considering the growing demand for food production from an expanding human population (Kluser and Peduzzi, 2007) and a growing demand specifically for pollinator-dependent crops (Aizen et al., 2008; Intergovernmental Science‐Policy
Platform on Biodiversity and Ecosystem Services, 2016). Understanding alternative sources of pollination and methods of supporting wild pollinator populations is critical to ensure the future of global food security.
45 In natural ecosystems worldwide, pollinators are keystone species with more than
90% of flowering plants relying on animal pollination for reproduction
(Intergovernmental Science‐Policy Platform on Biodiversity and Ecosystem Services,
2016). In general, a small minority of common bee species that are relatively robust to agricultural intensification provide most crop pollination services, with threatened species rarely visiting crops. Thus, other non-crop visiting pollinators must be considered in conservation measures, because they will not be supported by the same methods as robust, generalist crop-visiting species (Kleijn et al., 2015). In most regions of the world, little baseline data exist for bee communities to compare with current communities
(Sheffield et al., 2013a) so there is a need for natural history studies and pollinator monitoring programs to create a better understanding of wild pollinator biology and populations.
More than 75% of the world’s leading food crops rely on animal pollination for maximum quality and yield (Klein et al., 2006). Multiple crops exhibit a positive correlation between fruit or seed set and species richness of pollinator community, i.e. coffee (Klein, 2009), sunflower (Sardiñas and Kremen, 2015), and pumpkin (Hoehn et al., 2008). A higher species richness of wild insects on farms is associated with higher abundance of flower visitors and enhanced crop pollination (Garibaldi et al., 2014).
Larger scale production of many pollinator-dependent crops to sustain production growth has led to reductions in natural or semi-natural areas near agricultural lands (Garibaldi et al., 2014), which decreases the richness and abundance of wild pollinators such butterflies, flies, wasps and bees (Winfree et al., 2011), leading to diminished crop
46 pollination services (Garibaldi et al., 2011). Isolation from important floral and nesting resources in natural areas are likely to be the most important factors explaining the decline in abundance and diversity of native bees and corresponding loss in pollination services, as well as the use of insecticides and herbicides in conventional agriculture
(Kearns et al., 1998; Kremen et al., 2002). The current global trend in agriculture degrades agro-ecosystems, natural habitats and the ecosystem services these areas provide (Tilman et al., 2001). In terms of pollination services, these trends will exacerbate farmers’ reliance on managed pollinator species unless native pollinator species can be restored.
To achieve adequate native insect pollination to maximize crop yields, a farm landscape must provide sufficient nesting and floral resources to support pollinators throughout the year. One commonly suggested method of improving conditions for pollinators in agro-landscapes is planting alternative floral resources, i.e. wildflower strips or hedgerows, to increase floral diversity, food resources and potential nesting resources (Carreck and Williams, 2002; Garibaldi et al., 2014; Heard et al., 2007;
Kremen et al., 2004). Wildflowers and hedgerows can provide food and nesting resources for bees and other pollinators, as well as predatory and parasitic insects, enhancing species richness and abundance of these beneficial insects (Garibaldi et al., 2014). The effects of this method of on-farm pollinator enhancement on biodiversity conservation and crop pollination remains unstudied for many crop systems and different ecological contexts (Morandin and Kremen, 2013; Winfree, 2010).
47 My study focused on watermelon, Citrullus lanatus L., a monoecious crop grown on 3,035 hectares in South Carolina in 2017 and worth $33.7 million in value of production (2017 State Agricultural Overview , 2017). Watermelon is the largest acreage vegetable crop grown in South Carolina, with commercial production centered in the lowcountry and sand hills region of the upstate (South Carolina Department of
Agriculture, 2019). The use of honey bee hives to provide pollination services to this crop is common practice, and much of the available extension information and other publications cite honey bees as the primary watermelon pollinator (i.e. (Morse and
Calderone, 2000; UGA, 2017). However, research in California and New Jersey recognizes the contribution of a broad suite of native bees to watermelon pollination, many of which are more efficient pollinators on a per-visit basis than honey bees
(Kremen et al., 2002; Winfree et al., 2008). No previous studies of this kind have investigated the wild pollinators of watermelon in this region, and the only previous studies or surveys on bees or pollinators in South Carolina are the state records from
Droege et al. (2011) and two studies on cavity nesting bees (Horn and Hanula, 2004;
Jenkins and Matthews, 2004). The objectives of this research are to (1) inventory the wild pollinator assemblage of watermelon in South Carolina to better understand the pollination system in this region, (2) inform management decisions for habitat requirements based on the specific pollinator community composition, and (3) determine if providing higher floral diversity on farms by transplanting wildflowers and retaining weedy flowers affects species richness of the pollinator community.
MATERIALS AND METHODS
48 Study species
Watermelon ( Citrullus lanatus L.) is a monoecious flowering crop that is entirely dependent on insect pollinators to set fruit (Delaplane et al., 2000). Young watermelon seedlings were planted in fields between March and May, with peak flowering occurring in June and July, and a total flowering period of approximately two months. Watermelon flowers open one to two hours after sunrise, close between noon and 1330 EDST depending on weather conditions, and do not reopen once closed (Mcgregor, 1976, M.
Jenkins, personal observation). Multiple varieties were planted in my study sites, including both triploid seedless variety SP7 and diploid seeded varieties Charleston Grey,
Crimson Sweet and Sugar Baby.
Study sites
The study was conducted in coastal and central South Carolina in Charleston,
Barnwell, and Bamburg Counties in the Southern Coastal Plain and Middle Atlantic
Coastal Plain ecoregions of the southeastern US. In 2016, six watermelon fields served as independent sites at Clemson University Coastal Research Center in Charleston, South
Carolina, Clemson University Edisto Research Center in Blackville, SC and a commercial grower’s field in Olar, SC. The fields were separated by at least 500 m and ranged in size from 0.1 – 2 hectares. Three fields were conventional monoculture watermelon fields and three fields were “diversified” fields, containing wildflowers and/or other co-flowering crop species intermixed with the watermelon crop. Wildflower plantings consisting of thirteen species of native wildflowers (Supplementary Info Table
2.10) were transplanted into the three “diversified” fields in four 2 meter long sections
49 within each row in the spring of 2016. The wildflowers flowered before, during, and after the watermelon flowering period of each field. The fields adjacent to all study sites contained a range of crops consisting of tomatoes, corn, watermelon, squash, cantaloupe and cucumber but were separated from my fields by at least 100m.
In the 2017 study, I paired fields together in blocks to account for environmental heterogeneity in the landscape, climate, and other factors that could also influence pollinator communities and behavior. Five treatment fields were paired with five control fields in similar locations and with similar conditions in terms of chemical spraying, flowering period of watermelon, and field size. Six of these fields were at the Clemson
Coastal Research Center in Charleston SC, two fields at Clemson Edisto Research Center in Blackville, SC, and two at a small polyculture farm on John’s Island, SC. Each treatment field had one ~60m x 1m row of wildflowers on one edge of the field that flowered before, during and after the watermelon flowering period. The wildflower strips consisted of 20 plots of four wildflower species transplanted as seedlings into plots along a row. Each of the four flower species comprised five 1m 2 plots with 20 plants per plot, separated by 1m between each plot. The wildflower seeds were not treated and were germinated from seed in February and March at the USDA Vegetable Laboratory in
Charleston, SC in a greenhouse and outdoors. They were transplanted into each treatment field in April or May 4-6 weeks before watermelons were transplanted into each field so that they would be flowering before watermelon. The four wildflower species, Yellow
Zinnia (cardinal) ( Zinnia elegans ), Indian blanket ( Gaillardia pulchella ), Plains
Coreopsis ( Coreopsis tinctorial ) and Sulphur Cosmos ( Cosmos sulphureus ), were chosen
50 based on drought tolerance, hardiness, length of flowering period, difference in flowering phenology, and my observations in watermelon fields in 2015 of their attraction to a wide diversity of pollinators. The control watermelon fields did not contain wildflower strips.
In 2018, ten fields in Charleston and Barnwell Counties, SC were included in the study. All fields this year contained wildflowers but differed in wildflower location; wildflowers were either in the field or near the field within 50-100m. Five fields were located on two small polyculture farms on John’s Island, SC, at Clemson Edisto Research
Center in Blackville, SC and Clemson Coastal Research Center in Charleston, SC with multiple crops present and weedy flowers and wildflowers within 50-100 m of the field edges. Zinnia elegans, Verbena hastata, and Monarda fistulosa, made up the majority of the wildflower species near these fields. Three fields were also located at the Clemson
Coastal Research and Education Center in Charleston SC and contained transplantings of four wildflower species ( G.pulchella, Z.elegans, C. tinctoria, C.sulphureus ) in 60m x 1m strips along one edge of each field, as was done in treatment fields in 2017. In 2016-
2018, two to three honey bee hives were placed near all the fields. No commercial
Bombus impatiens colonies were placed near the fields.
Pollinator collection
To determine the effect of different treatment types on fields in terms of pollinator biodiversity and community composition, I collected insects visiting watermelon flowers using aerial nets in 21 watermelon fields in South Carolina. All insects were frozen, pinned, and identified by Mimi Jenkins and Sam Droege (US Geological Survey Native
Bee Inventory and Monitoring Lab, Beltsville, Maryland). From 2015 - 2018, I collected
51 insects visiting open watermelon flowers and wildflowers throughout the field for 20 - 30 minutes on multiple days per field, in varying weather conditions but always over 70 degrees F. I focused on species that are impossible or difficult to identify in the field such as Lasioglossum spp., Megachile spp., and Halictus spp. and stopped collecting individuals of certain common species ( Bombus impatiens, Bombus fraternus, Melissodes bimaculata ) whenever ~50 specimens had been collected and I became more certain of my field identification. Due to varying numbers of volunteers available, distances to fields, and weather conditions, sampling effort differed among fields.
In 2016, I also collected insects using plastic cups, or “bee bowls”, for ten days in two fields. The bowls were provided by Sam Droege (USGS Bee Monitoring and
Inventory lab), were painted with UV reflecting paint (blue, white and yellow), filled with soapy water, and collected into alcohol after 24 hours on rain-free days. Thirty bowls were mounted onto 30.5 cm tall stakes in each field and pounded into the ground along the rows of watermelon at random locations throughout the fields. This allowed the bowls to remain at canopy level. Insects were collected into 80% ethanol after 24 hours in the field and the cups were refilled with soapy water.
Analysis
I considered insects collected from the bee bowls separate from net collected insects. Due to the sampling effort differences that affected the relative abundance of species, I created a species accumulation curve to estimate species richness based on sampling events. This allowed me to determine if I was close to reaching the true species richness within the pollinator community. Accumulation curves record how many species
52 are collected during sampling as more samples or individuals are added to the collection
(Gotelli and Colwell, 2001). I also estimated species richness for each field with individual rarefaction, which uses an algorithm to repeatedly resample individuals or samples from the total pool in the collection and generate a rarefaction curve (Sanders,
1968; Simberloff, 1978). This curve approximates the number of species for given subsample sizes (Gotelli and Colwell, 2001). I used this curve to account for differences in number of individuals collected at locations in each year of sampling to compare species richness between treatment and control fields. All rarefaction estimates were obtained using PAST (Hammer et al., 2001).
To determine similarity of community composition, I created Jaccard’s similarity matrices by converting the data into presence/absence data. Similarity between community assemblages were calculated using the Jaccard incidence-based similarity index which ranges from 0 (no overlap between assemblages) to 1 (total overlap) and was calculated using PAST (Hammer et al., 2001). Jaccard indices were calculated using all species collected visiting the six most important floral species ( C.lanatus, C.tinctoria,
G.pulchella, C.sulphureus, Z.elegans, V.hastata ).
RESULTS
From 2015-2018, I collected 2,696 insects, using aerial nets, in 21 watermelon fields in South Carolina. The number of sampling events per field ranged from one to fourteen times (mean 6.31 SE ± 0.72) (Table 2.1). Since the focus of the study was to describe the pollinator community of C. lanatus, I collected 1,669 specimens (61.89%) from watermelon, and 1,006 total specimens from five wildflower species: 238
53 specimens (8.83%) from Coreopsis tinctoria , 178 (6.6%) from Cosmos sulphureus , 348
(12.91%) from Gaillardia pulchella , 216 (8.01%) from Zinnia elegans and 47 (1.74%) from Verbena hastata . In 2016, I collected an additional 294 specimens using bee bowls at two fields in 2016. I also recorded 299 observations of species able to be identified by sight in the field or using photography (i.e. Lepidopterans, Bombus spp., Xylocopa spp.,
Melissodes bimaculata ).
Sam Droege took high quality photographs of several of my specimens and included them on his website
(https://www.flickr.com/photos/usgsbiml/38016647111/in/album-72157688547596404/).
A small sample of the voucher specimens are housed in the Smithsonian Institution’s
National Museum of Natural History in Washington, DC and all other voucher specimens are housed in the Clemson University Arthropod Collection in Clemson, SC.
I identified 82 total insect species (65 species that were collected with nets, 17 species that were observed only) on watermelon fields in my study from C.lanatus,
C.tinctoria, C.sulphureus, G.pulchella, Z.elegans, and V.hastata flowers. I identified 59 insect species visiting C.lanatus specifically in 21 fields from 2015 - 2018, 91% of which are native bees from 4 families (Halictidae, Megachilidae, Apidae, Colletidae) (Table 2.2,
Figure 2.1). Several species of skippers (Hesperiidae), syrphid flies, including Palpada sp. and Toxomerus sp., as well as a few butterfly ( Agraulis vanillae) and wasp species
(Campsomeris sp .) comprised the majority of the non-bee specimens and observed visits to watermelon flowers. This compares to pollinator communities of watermelon consisting of 39 and 31 insect species from studies in the northeastern US and Central
54 Valley of California, respectively, on about 17 farms each (Kremen et al., 2002; Rader et al., 2013). The number of bee species collected per year visiting C. lanatus in my study was similar across years—with 35, 34 and 33 species collected in 2018, 2017 and 2016 respectively. Nomada vegana, a small cleptoparasitic bee, is a new state record for South
Carolina.
I identified 60 insect species collected with nets from the wildflowers I transplanted in the fields ( C. tinctoria , C. sulphureus , G. pulchella , Z. elegans ) and the common “weedy” V. hastata (Table 2.3, Figure 2.1). The four wildflower species transplanted into fields attracted a mean of 25.75 SE ± 1.3 native bee species, in addition to honey bees and many other non-bee beneficial insects. Zinnia elegans attracted more non-bee species than the other three wildflower species, including Monarch butterflies
(Danaus plexippus ) and three swallowtail butterfly species ( Papilio spp.). Of the 59 total watermelon visitor species collected, 38 species (64%) were also collected visiting the five focal wildflower species.
In 2016, I observed a slightly higher species richness of watermelon visitors in treatment fields (16.3 SE ± 0.88) than in control fields (11.6 SE ± 3) with a range of 6 -
18 species. In 2017, I also observed a slightly higher species richness of watermelon visitors in treatment fields (16.4 SE ± 2.3) compared to control fields (15.2 SE ± 1.7), with a range of 10 - 23 species. In 2018, I observed a slightly higher species richness of watermelon visitors in fields with wildflowers nearby (15.2 SE ± 1.9) compared to fields with wildflowers within the field (13.5 SE ± 3.8) (Figure 2.2). I collected a mean of 22.3
SE ± 4.4 and 27 SE ± 4.2 pollinator species at treatment fields on all floral species in
55 2016 and 2017, respectively, so the overall pollinator community species richness was higher as floral diversity increased. In 2018, I found a higher species richness when all floral species were included in fields with wildflowers within the field (26.8 SE ± 4) compared to fields with wildflowers nearby (20.5 SE ± 3.5). I collected more specimens in treatment fields (305 in 2016, 727 in 2017) than in control fields (147 in 2016, 166 in
2017), which might be a result of a higher abundance of insects when more floral species were present, or the increased sampling effort in some treatment fields due to less traveling distance and other factors.
The most abundant species in the collection is Lasioglossum callidum with 767 specimens (27% of all specimens collected) which was collected at seven out of ten fields in 2017 and 2018, and at all six fields in 2016. It was collected on C. lanatus , C. tinctoria , C. sulphureus, G. pulchella , Z. elegans, and V. hastata . Because tiny bees and other insects that are impossible to identify to species in the field were prioritized during collection, the amount I collected does not necessarily correlate with abundance in nature; however, this pollinator group (tiny bees/ Lasioglossum spp.) was also the most frequent visitor of watermelon flowers (Chapter 1).
Another species that I widely observed and collected pollinating watermelon was
Bombus impatiens with 137 specimens or 5% of total specimens (this species was not collected as often once they were verified because they are more easily identified in the field). It was observed in 5 out of 6 fields in 2016 and 9 out of 10 fields in 2017 and
2018. It was collected on C. lanatus , C.sulphureus , G.pulchella , Z.elegans , V.hastata ,
Rudbeckia hirta and Monarda fistulosa . A third common watermelon pollinator was
56 Melissodes bimaculata with 93 specimens or 3.4 % of the specimens (also more easily identified in the field so not as frequently collected). It was observed and collected in 3 out of 6 fields in 2016, 7 out 10 fields in 2017, and 5 out of 10 fields in 2018. It was collected visiting C. lanatus , C.tinctoria, C.sulphureus , G.pulchella , Z.elegans , and
V.hastata .
During 2016, 2017 and 2018, most of the 65 total insect species collected off the six floral species listed above were collected less than ten times. In my collection, 19% of the species are only represented by one specimen, 56% are represented by <10 specimens, 83% are represented by <50 specimens, and only 16% had >50 specimens.
In 2016, I collected 20 bee species with bee bowls, which were all also collected with nets (Table 2.4). The community composition of these specimens differed from the net collected specimens, although there were only 294 specimens collected in this manner compared to 2,696 with nets. Lasioglossum longifrons made up 39% of the specimens collected in the bee bowls, as opposed to 0.8% out of 2,695 specimens collected in nets on all fields. Lasioglossum callidum made up 19% of the bee bowl specimens and 28% of the net collected specimens. Melissodes communis and M. bimaculata made up 8% and
7% of the bee bowls and 4% and 3% of the net collected specimens, respectively.
Hylaeus ornatus was a rare species with only 2 specimens in the bee bowls at one field and 3 specimens collected in nets. Melitoma taurea and Ptilothrix bombiformis were also rare species in my study, with only 1 specimen collected by net and 1 from bee bowls of each.
57 The bees collected in my study range in sociality and nesting biology, with most species being solitary, parasocial, or subsocial (53%), less being primitively eusocial
(34%), a small percentage being cleptoparasites (12.5%) and A.mellifera being the only highly eusocial species. C, one third of species (33%) are solitary ground nesters, 28% are social ground nesters, 20% are cavity nesters, 12.5% are cleptoparasites, and 6% are bumble bees. In terms of the number of specimens collected from each guild, social ground nesters were the most collected (52% of the total specimens), followed by solitary ground nesters (22%), cavity nesters (13.5%), bumble bees (9.5%) and cleptoparasites
(2.5%).
Cleptoparasitic bees, or brood parasitic bees, invade the nests of non-conspecific host bee species, oviposit in natal cells, and their larvae develop on the provisions intended for the host’s larvae (Rozen, 2001). I collected cleptoparasites at 7 out of 8 treatment fields and none of the control fields in 2016 and 2017, and at 2 out of 6 fields with wildflowers nearby and 3 out of 4 fields with wildflowers within the field. I collected 8 species of cleptoparasitic bees visiting the wildflowers and 6 species visiting watermelon, with 67 specimens collected over four years. These bees are Coelioxys sayi, a brood parasite of Megachile spp. (Sheffield et al., 2003); Triepeolus concavus, a brood parasite of Svastra obliqua obliqua; T. lunatus, most likely a brood parasite of
Melissodes bimaculata; T. remigatus, a brood parasite of Xenoglossa strenua; and T. simplex, a brood parasite of Peponapis pruinose (Rightmyer, 2008); Nomada vegana, and
N.fervida, brood parasites of Agapostemon spp., Halictus spp., Lasioglossum spp. and
Colletes spp. (Sheffield et al., 2003); and Sphecodes sp., a brood parasite of mostly other
58 Halictinae including Lasioglossum spp. (Sheffield et al., 2003). All of the host species of the cleptoparasites are common watermelon pollinators, with the exceptions of Svastra obliqua obliqua, an Asteraceae specialist, and Peponapis pruinosa and Xenoglossa strenua, which are both oligolectic squash specialists. P. pruinosa was collected in 2016 on squash flowers in one field where squash was present near watermelon flowers.
Svastra obliqua obliqua was collected in seven fields on all four of the transplanted wildflower species, especially Gaillardia pulchella.
Similarity between control fields ranged from Jaccard indices of 0.28 SE ± 0.04 to
0.40 SE ± 0.03 in 2016 and 2017, respectively. Mean similarity between treatment fields ranged from 0.30 SE ± 0.04 to 0.25 SE ± 0.03 in 2016 and 2017, respectively (Table 2.5,
2.6). Pollinator community similarity within treatment types differed significantly in
2017, with treatment groups having a higher mean similarity index than control groups (F
(1,18)=10.19, p=0.005) (Table 2.7). Among paired treatment and control fields in 2017, the mean Jaccard similarity index was 0.30 SE ± 0.02 (Table 2.8). In 2018, similarity between fields that had wildflowers within the field was slightly higher (0.35 SE ± 0.07) than fields with wildflowers nearby (0.25 SE ± 0.04). Among fields studied across multiple years, the mean Jaccard similarity index was 0.41 SE ± 0.04 (Table 2.9).
The species accumulation curve, which includes all 167 sampling events at 28 watermelon fields from 2015 - 2018, shows no evidence of reaching an asymptote, implying that the sampling effort was insufficient to determine the real species richness of the overall community (Figure 2.3). The individual species rarefaction curves show that for some sites, the curve was flattening because of a higher number of specimens
59 collected, nearing an asymptote and indicating an approach to the true richness of that site’s pollinator community (Figure 2.4, 2.5). In addition, species rarefaction curves show how sites differed in the pollinator community species richness, based on whether the
95% confidence intervals overlap. These graphs reiterate that the treatment fields had a higher number of sampling events and specimens collected compared to control sites in
2016 and 2017, and fields with wildflowers within the field had a higher level of sampling effort compared to fields with wildflowers nearby in 2018.
DISCUSSION
Overall, the biodiversity of the pollinator community was higher in watermelon fields with increased floral diversity. Nearly twice the number of pollinator species was collected on watermelon fields with wildflowers compared with control fields. In addition, the species richness of pollinators visiting watermelon flowers was slightly higher in fields with higher floral diversity than those with only watermelon flowers.
These results support management recommendations to provide additional floral resources for native pollinators, even on a small scale such as a small wildflower strip with four wildflower species, or by retaining weedy flowers growing in ditches and along field edges. Agroecosystems typically have lower bee diversity than surrounding natural habitats (Cane et al., 2006; Klein et al., 2007; Kremen et al., 2002; Larsen et al., 2005) but the presence of hedgerows, natural borders and corridors in agricultural landscapes has previously shown positive effects on bee diversity and abundance (Greenleaf and
Kremen, 2006; Pywell et al., 2006; Shepherd and Ross, 2003). Bee species richness was lower in landscapes dominated by intense agricultural use compared with landscapes with
60 forests or natural areas nearby, and proximity to natural habitat with abundant floral resources had positive impacts on bee species richness (Sheffield et al 2013). The lack of intense agricultural land use yielding a more heterogeneous landscape matrix with forests and salt marshes near most of the fields likely influenced the observed bee species richness on watermelon fields in my study.
The current reliance on a small number of managed species, mostly the honey bee, for pollination services, is unsustainable (Kremen, 2008; Winfree et al., 2007), especially because managed colonies of honey bees have declined about 50% since the
1950s (National Research Council (U.S.), 2007). Diversity in a community has multiple benefits including stability, productivity and reduced susceptibility to invasion (Cardinale et al., 2006; Duffy et al., 2007; Hooper et al., 2005). In many regions of the world, baseline data about the biodiversity of pollinator communities of native plants and crops are lacking (Sheffield et al., 2013). An increased diversity in the pollinator community improves stability of pollination services for growers to produce pollinator-dependent crops because a diverse assemblage varies in behavior, morphology and other life history traits, leading to complementary resource use (Albrecht et al., 2012; Blüthgen and Klein,
2011). Wild bees improve seed set, quality, shelf-life and commercial value of many crops (Bartomeus et al., 2014; Hoehn et al., 2008; Klatt et al., 2013; Mallinger and
Gratton, 2015; Winfree et al., 2011) and are more efficient pollinators of certain crops including watermelon (Kremen et al., 2004; Rader et al., 2016; Winfree et al., 2008).
Many native bees forage earlier in the morning than honey bees can and in rain, especially bumble bees which can thermoregulate (Williams et al., 2014). In addition,
61 many non-bee pollinator taxa have longer temporal activity ranges and can forage in more adverse weather conditions than bees (McCall and Primack, 1992; Owen and
Gilbert, 1989; Primack and Primack, 1978). Non-bee pollinators such as syrphid flies, bombyliid flies, wasps and lepidopterans are less vulnerable to changes in land use than wild bees, because they often rely less on surrounding land conditions and have different nesting requirements and life histories as larvae and adults (Rader et al., 2016).
A thriving community of insects can have ripple effects in ecosystems, supporting many insectivorous species, serving as an important foundation for other trophic levels, and supporting ecosystem function (Wilson 1971, Wilson 1987, Losey 2006). Pollinators in particular are keystone species, playing a critical role in ecosystems worldwide in native plant and crop pollination (Biesmeijer et al., 2006; Klein et al., 2007). Native bees alone can provide sufficient pollination services in some systems, including watermelon in Pennsylvania and New Jersey, acting as insurance against continued honey bee declines (Winfree et al., 2008). Furthermore, native biodiversity of pollinators buffers crop pollination services against climate change because of different responses to climate change. Pollination services from honey bees are expected to decline substantially under the most extreme Intergovernmental Panel on Climate Change scenarios while native species are expected to increase (Rader et al., 2013). Lastly, an increased abundance and species richness of native bees can vastly improve honey bee per-visit efficiency and seed set through behavioral interactions that cause honey bees to move more quickly between male and female crop rows than they normally would (Greenleaf and Kremen, 2006).
62 The varying degree in sampling effort between fields in my study, leading to a wide range in the number of specimens collected per field, makes it necessary to question whether differences in species richness were driven by this sampling difference or a real difference occurring in nature. Rarefaction allows for meaningful comparisons of species richness while considering sampling effort (Gotelli and Colwell, 2001) and is recommended over traditional diversity indices. This is especially true in arthropod assemblages that typically involve large data sets in terms of number of individuals, number of samples, and number of species collected (Buddle et al., 2005). The individual rarefaction curves show that the observed species richness of the fields with smaller sample sizes tend to fall within the 95% confidence intervals of the expected species richness of the fields with larger sample sizes. This overlapping among the observed species richness and 95% confidence intervals (except between certain treatment fields) shows that species richness does not differ significantly (P<0.05) between fields, and any difference in observed species richness is driven by a difference in sampling effort
(Simberloff, 1978). The only exceptions where the observed species richness clearly does not overlap with the confidence intervals of another field site are in 2018, where two of the fields with wildflowers nearby (NEAR.ROSE2, NEAR.F9) have significantly higher species richness than two fields with wildflowers within the field (WIN.4G, WIN.EREC)
(Figure 2.5). These samples differ in species richness in ways that cannot be accounted for entirely by differences in abundance and sampling effort (at P<0.05) (Gotelli and
Colwell, 2001).
63 More sampling of these watermelon fields is necessary to approach the real species richness of the pollinator communities there, as shown by the species accumulation curve that does not approach an asymptote as more samples were collected.
Insufficient sampling is common when assessing the biodiversity of many biological communities, especially arthropods (Buddle et al., 2005; King and Porter, 2005). Many of the species in my study were collected once (19%) or fewer than ten times (56%), but rare species commonly make up large proportions of bee faunas (Michener, 1979;
Williams et al., 2001). Nevertheless, the proportion of singletons indicates that more intensive and prolonged sampling would reveal more species. The pollinator fauna of agroecosystems can be diverse and challenging to thoroughly sample, and sampling effort required to detect true species richness varies depending on field conditions (Russo et al.,
2015). Additionally, there was a large difference in sampling effort amongst fields in my study, due to varying distances and travel time required.
A community of 59 insect pollinator species of watermelon, mostly native bees from 4 families, were recorded that have previously been unreported in the literature for this region. Many publications report that honey bees ( Apis mellifera) provide most of the pollination services to watermelon, and that it is essential to place honey bee hives close to watermelon fields to ensure crop pollination (Morse and Calderone, 2000; UGA
Extension, 2017). Watermelon growers are aware of honey bees and bumble bees pollinating their watermelon crop, but many are unaware of the multitude of other pollinator species (M. Jenkins, personal communication with farmers). Previous studies have shown that many native bee species are more efficient pollinators of watermelon
64 flowers because they deposit more pollen on watermelon stigmas per visit, tend to forage earlier in the morning when watermelon stigmas are more receptive, and have a higher visitation rate due to faster foraging behavior than A. mellifera (Campbell et al., 2018;
Kremen et al., 2002; Stanghellini et al., 2002). More than half (64%) of the watermelon pollinator species I collected were also collected on one or more of five wildflower species, demonstrating that social colonies of bees, solitary bees, and other insects such as syrphid flies and butterflies use multiple floral species as resources in watermelon fields in addition to the crop flowers.
The similarity in species composition was low between fields and was significantly more similar among control fields compared with similarity among treatment fields in 2017. Thus, the 21 fields included in my study had relatively dissimilar pollinator communities, reflecting a wide range of communities even between sites that were geographically close (~800 m away). A significantly higher similarity in the pollinator community species composition between control fields in 2017 might be due to the lower floral diversity which meant that insects were being collected from only one plant species (watermelon). The relatively low level of agricultural intensity in my area, smaller field sizes and species richness of flowering crops and weedy flowers in surrounding fields might have led to the wide range of pollinator guilds I observed, high species richness of watermelon pollinators in some fields, ability to detect rare species, and large contribution of wild bees to the pollination services, similar to the results of
Winfree et al. (2008). These small scale diversified agro-landscapes are globally threatened by agricultural intensification (Tilman et al., 2001), so this region should focus
65 on limiting development or intensification of agriculture to ensure the future of pollinator biodiversity.
The presence of wildflowers in watermelon fields increased species richness and attracted species that were not collected at control sites. For example, cleptoparastic bees were collected visiting watermelon and wildflowers only at treatment fields (and in 7 out of 8 of them) in 2016 and 2017 and at both treatment types of fields with wildflowers in
2018. Most of the 67 cleptoparasitic specimens (82%) were collected visiting the wildflower species. These species exhibit a stabilizing role by causing competition among hosts (Combes, 1996) and represent the apex of bee communities (Sheffield et al.,
2013a). Habitat disturbance that affects species richness or fecundity of non-parasitic bee taxa via a decline in resource availability is often first noticed in the relative abundance and diversity of the cleptoparasites. Sites with diverse and abundant cleptoparasite assemblages have lower dominance than in sites with fewer cleptoparasites, and highly managed agricultural fields support much lower abundance and diversity of cleptoparasites compared to areas with more natural habitat. The cleptoparasitic guild responds in ways that are representative of the entire bee community and probably serve as sensitive indicator taxa for assessing the status of ecosystems (Sheffield et al., 2013a).
Diversity data alone may not always reflect habitat quality for bees, especially at intermediate levels of disturbance, and life history analyses of bee community diversity might be critical because bees make up a diverse assemblage of sociality, life histories, and nesting biology (Michener, 2007), making it challenging to generalize about the group as a whole (Sheffield et al., 2013a). The diversity of cleptoparastic bees only at
66 sites with wildflowers in my study reflects the habitat quality necessary to support pollinator communities that include these important stabilizing species. Additionally, most of the butterfly species (9 out of 12) in this study visited wildflowers and not watermelon flowers, again showing the effect that a relatively small area of wildflowers in an agricultural field can have to promote biodiversity.
The proportion of bee guilds in a community often reflects the availability of floral and nesting resources in a particular area. For example, in New York City parks and gardens, where the nesting resources consist of trees, wood piles, sheds, homes and fences and little soil substrate due to disturbance and compaction, most specimens collected were cavity nesters with a small proportion of soil nesters (Matteson et al.,
2008). In contrast, soil-nesting bees were more commonly collected in rural areas (Giles and Ascher, 2006), and in a similar study, solitary ground nesting bees were most abundant in agriculturally dominated landscapes, and cavity nesters and cleptoparasites least abundant in intense agricultural lands (Sheffield et al., 2013a). Several studies report a decrease in the abundance of belowground nesters and an increase in the number of aboveground nesters relative to the amount of impervious surfaces, related to urbanization or land development (Cane et al., 2006; Geslin et al., 2016; Matteson et al.,
2008; Winfree et al., 2009).
Most (52%) of the bee specimens I collected are social ground nesters. In terms of number of species per guild, solitary ground nesters made up the largest proportion of species (33%), social ground nesters made up slightly fewer species (28%) and cavity nesters made up 20% of species. Among the bees collected from the wildflowers, 44%
67 were social ground nesters and 29% were solitary ground nesters, and among the watermelon bee assemblage, a higher proportion were social ground nesters (57%) and
18% were solitary ground nesters. Lasioglossum callidum is a primitively social ground nester (most likely, Jason Gibbs, personal communication), and made up 27% of the total collection with 734 specimens collected. Halictus poeyi , a facultatively social ground nester, was the next most frequently collected species making up 11% of the total specimens. The prevalence of these species in my fields and my collecting methods which emphasized smaller, less identifiable species likely resulted in the large proportion of social ground nesters.
Management efforts that consider the nesting requirements of these different bee guilds is critical to supporting native bee populations. Most native bees are solitary ground nesters (Cane, 1991), and due to small size and forage range (usually within 500m of the nest site) they depend on adequate specific soil conditions to raise offspring
(Choate et al., 2018). These digger bees usually excavate nesting burrows within exposed patches of soil or cut banks, often in aggregations (Michener, 2000), suggesting that nesting females may select sites with particular surface or edaphic qualities (Cane,
1991). Nesting tunnels vary greatly between species, but most species nest within 40 to
50 cm of the surface of well-drained soils (Cane, 1991) and have preferences for different soil compositions and moisture levels (Wcislo and Engel, 1996), vegetative cover, and proximity to shelter such as wood field margins. Given the shallow depth of many brood cells (<30 cm below surface), no‐till farming may enhance populations of ground‐nesting bees (Roulston and Goodell, 2011). Tillage timing, depth, and method
68 probably have differential impacts on pollinators and pollination, but further studies are required to verify this (Garibaldi et al., 2014). Drip irrigation may also be preferable over flood irrigation to avoid flooding nests but irrigation in general can make the soil easier to penetrate, thereby promoting wild insect nesting (Julier and Roulston, 2009).
Some of the digger bee species collected in my fields include Lasioglossum pilosum, which nests in open sand dunes, L.lustrans, which nests in clay soil
(Bartholomew et al., 2006), Augochlorella aurata, which nests in well drained clay or clay/loam soils (Mueller, 1996; Packer, 1990), and Halictus rubicundus, which nests in sandy-loamy soil. Ptilothrix bombiformis, a Hibiscus specialist which was collected only twice in my study, nests near coastal marshes and uses water to dampen hard clay soils to construct its nest (Rust, 1980). Many ground nesting bees have not been studied or studied in more than one geographic area to understand their natural history.
Leafcutter bees ( Megachile spp.), part of the cavity nesting guild that visited both watermelon and wildflowers, have complex nesting habits, using a wide variety of foreign plant materials, mud and resin for construction of brood cells (Michener, 2000).
They typically construct brood cells with pieces of fresh leaves in pre-existing cavities, including wood-boring beetle holes, and artificial nest tunnels (Sheffield et al., 2003).
Also in the cavity nester guild and visitors of watermelon and wildflowers were large carpenter bees ( Xylocopa spp.), robust bees that usually nest in solid soft wood but occasionally coarse, pithy hollow stems (Michener, 1979). The subsocial small carpenter bees ( Ceratina spp.) excavate nests in pithy dead stems which have been broken or
69 burned, exposing the soft pithy core (Sheffield et al., 2003). Augochlora pura is a solitary species that excavates rotting wood (Sheffield et al., 2003; Stockhammer, 1966).
Bumble bees nest on, above or below ground level in cavities depending on the species and thus require less disturbance of nearby natural areas to find nests. They are also more mobile than most other native bees, traveling 800m or more if necessary away from their nest (Hatfield et al., 2012). For example, The American bumble bee ( Bombus pensylvanicus), which visited both watermelon and wildflowers in my study, is commonly found in open grasslands and agricultural areas, tends to nest above the ground in tufts of long grasses, and thus is particularly susceptible to grassland habitat loss, intensive agriculture land-use, and management activities that neglect their nesting requirements. It is one of the most sharply declining bee species in North America, and is now found in 34% of its previously sampled US and Canada range (Colla et al., 2012).
Grassy, unmowed and undisturbed areas, and piles of hay provide nesting for this species.
Protected open land area would also likely benefit other bumble bee species that nest in pre-existing rodent holes, bird nests, or crevices. Mated bumble bee queens overwinter in rotting logs, loose soil or mulch and require undisturbed soil to survive (Williams et al.,
2014).
The most abundant species, Lasioglossum callidum, was collected at nearly all
(75%) of the watermelon fields and is in the genus that was the most frequent visitor to watermelon flowers in a related study (Chapter 1). Lasioglossum spp. deposits lower levels of pollen per visit on watermelon stigmas compared with other native bees like
Bombus spp. and Melissodes spp. (Kremen et al., 2002), but other factors such as floral
70 fidelity, foraging activity period, and especially visitation rates are important predictors of actual pollination (Vázquez et al., 2005). Thus, because Lasioglossum spp. had the highest visitation rate to watermelon flowers in treatment fields and were observed foraging at earlier times in the morning, they may be important pollinators of watermelon despite their relatively low per-visit pollen deposition. Lasioglossum spp. are probably nesting in sandy, loamy soil close to or within fields because their small size limits their foraging range (Gibbs, 2011; Greenleaf et al., 2007). Supporting their populations will depend on tillage and spraying practices that limit soil disturbance. Lasioglossum spp. were frequently observed and collected foraging on the wildflowers ( Z.elegans,
C.sulphureus, C.tinctoria, G.pulchella ) planted in the treatment fields, as well as weedy flowers or cover crops such as Verbena hastata and Trifolium spp., so they may benefit from higher floral diversity on agricultural fields (M. Jenkins, personal observation).
More research is needed on this speciose genus. Little is known of their natural histories which is necessary to develop management plans that can protect them.
Honey bees were collected and observed visiting watermelon flowers and all five of the other floral species. They were most frequently seen visiting V. hastata , a “weedy” plant commonly growing on field edges, and rarely seen visiting the other four wildflower species (M. Jenkins, personal observation). Thus, honey bees likely also reap the benefits of a more diverse floral community, and individual foraging workers probably learn to gather nectar from different floral species because honey bees exhibit high floral constancy (Free, 1963; Waser, 1986). Additional floral resources in agricultural fields benefit honey bees because a more diverse source of nutrients and
71 pollen improves the health and immune response of their brood (Alaux et al., 2010; Di
Pasquale et al., 2013). This may decrease their risk of overexposure to pesticides commonly sprayed in agricultural fields.
In addition to providing floral resources for pollinating insects, a wide variety of parasitic and predatory wasps, flies, orthopterans, and hemipterans were observed visiting the wildflowers as a nectar source, perching on wildflowers, and stalking or preying on pollinating insects. Wildflower strips and hedgerows are able to provide habitat and food resources for these beneficial insects that control crop pests (Balzan et al., 2016;
Ramsden et al., 2015) intrinsically valuable and rare or endangered species (Morandin and Kremen, 2013; Sardiñas and Kremen, 2015), and wildlife that rely on diverse insect communities as a food source (Staley et al., 2012).
CONCLUSION
My study is a first attempt to uncover pollinator biodiversity in watermelon agroecosystems in the southeastern US. I provide crucial data about the diversity of pollinator species in watermelon fields in South Carolina that can inform land management decisions and promote conservation of natural areas and corridors for pollinators that provide essential ecosystem services and other wildlife, especially with increasing land development and urbanization in the Charleston area. Additional research is needed to understand the complete assemblage of wild pollinators in this region, as most insect biodiversity studies require large sample sizes and many species natural histories remain unstudied (Sheffield et al., 2013). I found that a relatively small area of wildflowers transplanted into watermelon fields, or retaining weedy flowers on field
72 edges, helps support a rich community of wild pollinators that visit watermelon and wildflowers, as well as parasitic and predatory insects that can help control pest populations.
REFERENCES
2017 State Agricultural Overview, 2017.
Aizen, M.A., Garibaldi, L.A., Cunningham, S.A., Klein, A.M., 2008. Long-Term Global
Trends in Crop Yield and Production Reveal No Current Pollination Shortage but
Increasing Pollinator Dependency. Curr. Biol. 18, 1572–1575.
https://doi.org/10.1016/J.CUB.2008.08.066
Alaux, C., Ducloz, F., Crauser, D., Le Conte, Y., 2010. Diet effects on honeybee
immunocompetence. Biol. Lett. 6, 562–565. https://doi.org/10.1098/rsbl.2009.0986
Albrecht, M., Schmid, B., Hautier, Y., Muller, C.B., 2012. Diverse pollinator
communities enhance plant reproductive success. Proc. R. Soc. B Biol. Sci. 279,
4845–4852. https://doi.org/10.1098/rspb.2012.1621
Balzan, M. V., Bocci, G., Moonen, A.-C., 2016. Utilisation of plant functional diversity
in wildflower strips for the delivery of multiple agroecosystem services. Entomol.
Exp. Appl. 158, 304–319. https://doi.org/10.1111/eea.12403
Bartholomew, C., Prowell, D., Griswold, T., 2006. An Annotated Checklist of Bees
(Hymenoptera: Apoidea) in Longleaf Pine Savannas of Southern Louisiana and
Mississippi. J. Kansas Entomol. Soc. 79, 184–198.
Bartomeus, I., Potts, S.G., Steffan-Dewenter, I., Vaissière, B.E., Woyciechowski, M.,
73 Krewenka, K.M., Tscheulin, T., Roberts, S.P.M., Szentgyörgyi, H., Westphal, C.,
Bommarco, R., 2014. Contribution of insect pollinators to crop yield and quality
varies with agricultural intensification. PeerJ 2, e328.
https://doi.org/10.7717/peerj.328
Biesmeijer, J.C., Roberts, S.P.M., Reemer, R., Ohlemüller, M., Edwards, T., Peeters,
A.P., Schaffers, S.G., Potts, R., Kleukers, C.D., Thomas, J., Settele, W.E., Kunin,
W.E., 2006. Parallel declines in pollinators and insect-pollinated plants in Britain
and the Netherlands. Science (80-. ). 313, 351–354.
Blüthgen, N., Klein, A.-M., 2011. Functional complementarity and specialisation: The
role of biodiversity in plant–pollinator interactions. Basic Appl. Ecol. 12, 282–291.
https://doi.org/10.1016/J.BAAE.2010.11.001
Buddle, C.M., Beguin, J., Bolduc, E., Mercado, A., Sackett, T.E., Selby, R.D., Varady-
Szabo, H., Zeran, R.M., 2005. The importance and use of taxon sampling curves for
comparative biodiversity research with forest arthropod assemblages. Can. Entomol.
137, 120–127. https://doi.org/10.4039/n04-040
Butchart, S.H.M., Walpole, M., Collen, B., van Strien, A., Scharlemann, J.P.W., Almond,
R.E.A., Baillie, J.E.M., Bomhard, B., Brown, C., Bruno, J., Carpenter, K.E., Carr,
G.M., Chanson, J., Chenery, A.M., Csirke, J., Davidson, N.C., Dentener, F., Foster,
M., Galli, A., Galloway, J.N., Genovesi, P., Gregory, R.D., Hockings, M., Kapos,
V., Lamarque, J.-F., Leverington, F., Loh, J., McGeoch, M.A., McRae, L.,
Minasyan, A., Hernández Morcillo, M., Oldfield, T.E.E., Pauly, D., Quader, S.,
Revenga, C., Sauer, J.R., Skolnik, B., Spear, D., Stanwell-Smith, D., Stuart, S.N.,
74 Symes, A., Tierney, M., Tyrrell, T.D., Vié, J.-C., Watson, R., 2010. Global
biodiversity: indicators of recent declines. Science 328, 1164–8.
https://doi.org/10.1126/science.1187512
Campbell, J.W., Daniels, J.C., Ellis, J.D., 2018. Fruit Set and Single Visit Stigma Pollen
Deposition by Managed Bumble Bees and Wild Bees in Citrullus lanatus
(Cucurbitales: Cucurbitaceae). J. Econ. Entomol. 111, 989–992.
https://doi.org/10.1093/jee/toy008
Cane, J.H., Minckley, R.L., Kervin, L.J., Roulston, T.H., Williams, N.M., 2006. Complex
Responses Within A Desert Bee Guild (Hymenoptera: Apiformes) To Urban Habitat
Fragmentation. Ecol. Appl. 16, 632–644. https://doi.org/10.1890/1051-
0761(2006)016[0632:CRWADB]2.0.CO;2
Cane JH, 1991. Soils of ground-nesting bees (Hymenoptera: Apoidea): texture, moisture,
cell depth and climate. J. Kansas Entomol. Soc. 64, 406–413.
Cardinale, B.J., Srivastava, D.S., Emmett Duffy, J., Wright, J.P., Downing, A.L.,
Sankaran, M., Jouseau, C., 2006. Effects of biodiversity on the functioning of
trophic groups and ecosystems. Nature 443, 989–992.
https://doi.org/10.1038/nature05202
Carreck, N.L., Williams, I.H., 2002. Food for insect pollinators on farmland: insect visits
to flowers of annual seed mixtures. J. Insect Conserv. 6, 13–23.
https://doi.org/10.1023/A:1015764925536
Choate, B.A., Hickman, P.L., Moretti, E.A., 2018. Wild bee species abundance and
richness across an urban–rural gradient. J. Insect Conserv. 22, 391–403.
75 https://doi.org/10.1007/s10841-018-0068-6
Colla, S.R., Gadallah, F., Richardson, L., Wagner, D., Gall, L., 2012. Assessing declines
of North American bumble bees (Bombus spp.) using museum specimens.
Biodivers. Conserv. 21, 3585–3595. https://doi.org/10.1007/s10531-012-0383-2
Colla, S.R., Packer, L., 2008. Evidence for decline in eastern North American
bumblebees (Hymenoptera: Apidae), with special focus on Bombus affinis Cresson.
Biodivers. Conserv. 17, 1379–1391. https://doi.org/10.1007/s10531-008-9340-5
Combes, C., 1996. Parasites, biodiversity and ecosystem stability. Biodivers. Conserv. 5,
953–962. https://doi.org/10.1007/BF00054413
Delaplane, K.S., Mayer, D.R., Mayer, D.F., 2000. Crop pollination by bees. CABI
Publishing.
Di Pasquale, G., Salignon, M., Le Conte, Y., Belzunces, L.P., Decourtye, A.,
Kretzschmar, A., Suchail, S., Brunet, J.-L., Alaux, C., 2013. Influence of Pollen
Nutrition on Honey Bee Health: Do Pollen Quality and Diversity Matter? PLoS One
8, e72016. https://doi.org/10.1371/journal.pone.0072016
Droege, S., Ascher, J.S., Pickering, J., 2011. Discover life: Apoidea [WWW Document].
URL http://www.discoverlife.org/20/q?search=Apoidea.
Duffy, J.E., Cardinale, B.J., France, K.E., McIntyre, P.B., Thébault, E., Loreau, M., 2007.
The functional role of biodiversity in ecosystems: incorporating trophic complexity.
Ecol. Lett. 10, 522–538. https://doi.org/10.1111/j.1461-0248.2007.01037.x
Free, J.B., 1963. The Flower Constancy of Honeybees. J. Anim. Ecol. 32, 119.
https://doi.org/10.2307/2521
76 Garibaldi, L.A., Aizen, M.A., Klein, A.M., Cunningham, S.A., Harder, L.D., 2011.
Global growth and stability of agricultural yield decrease with pollinator
dependence. Proc. Natl. Acad. Sci. U. S. A. 108, 5909–14.
https://doi.org/10.1073/pnas.1012431108
Garibaldi, L.A., Carvalheiro, L.G., Leonhardt, S.D., Aizen, M.A., Blaauw, B.R., Isaacs,
R., Kuhlmann, M., Kleijn, D., Klein, A.M., Kremen, C., Morandin, L., Scheper, J.,
Winfree, R., 2014. From research to action: enhancing crop yield through wild
pollinators. Front. Ecol. Environ. 12, 439–447. https://doi.org/10.1890/130330
Geslin, B., Le Féon, V., Folschweiller, M., Flacher, F., Carmignac, D., Motard, E., Perret,
S., Dajoz, I., 2016. The proportion of impervious surfaces at the landscape scale
structures wild bee assemblages in a densely populated region. Ecol. Evol. 6, 6599–
6615. https://doi.org/10.1002/ece3.2374
Gibbs, J., 2011. Revision of the metallic Lasioglossum (Dialictus) of eastern North
America (Hymenoptera: Halictidae: Halictini)Revision of the metallic Lasioglossum
(Dialictus) of eastern North America (Hymenoptera: Halictidae: Halictini). Zootaxa
3073, 1–216.
Giles, V., Ascher, J.S., 2006. A survey of the bees of the Black Rock Forest Preserve,
New York (Hymenoptera: Apoidea). J Hymenopt Res 15, 208–231.
Gotelli, N.J., Colwell, R.K., 2001. Quantifying biodiversity: procedures and pitfalls in the
measurement and comparison of species richness. Ecol. Lett. 4, 379–391.
https://doi.org/10.1046/j.1461-0248.2001.00230.x
Goulson, D., Lye, G.C., Darvill, B., 2008. Decline and Conservation of Bumble Bees.
77 Annu. Rev. Entomol. 53, 191–208.
https://doi.org/10.1146/annurev.ento.53.103106.093454
Goulson D, Nicholls E, Botias C, Rotheray EL, 2015. Bee declines driven by combined
stress from parasites, pesticides and lack of flowers. Science (80-. ). 347.
Greenleaf, S.S., Kremen, C., 2006. Wild bees enhance honey bees’ pollination of hybrid
sunflower. Proc. Natl. Acad. Sci. U. S. A. 103, 13890–5.
https://doi.org/10.1073/pnas.0600929103
Greenleaf, S.S., Williams, N.M., Winfree, R., Kremen, C., 2007. Bee foraging ranges and
their relationship to body size. Oecologia 153, 589–596.
https://doi.org/10.1007/s00442-007-0752-9
Hammer, Ø., Harper, D.A.T., Ryan, P.D., 2001. PAST: Paleontological statistics
software package for education and data analysis. Palaeontologia Electronica.
Hatfield, R., Jepsen, S., Lee-Mader, E., Black, S.H., Shepherd, M., 2012. Conserving
Bumble Bees Guidelines for Creating and Managing Habitat for America’s
Declining Pollinators. Portland OR.
Heard, M.S., Carvell, C., Carreck, N.., Rothery, P., Osborne, J.., Bourke, A.F.., 2007.
Landscape context not patch size determines bumble-bee density on flower mixtures
sown for agri-environment schemes. Biol. Lett. 3, 638–641.
https://doi.org/10.1098/rsbl.2007.0425
Hoehn, P., Tscharntke, T., Tylianakis, J.M., Steffan-Dewenter, I., 2008. Functional group
diversity of bee pollinators increases crop yield. Proc. R. Soc. B Biol. Sci. 275,
2283–2291. https://doi.org/10.1098/rspb.2008.0405
78 Hooper, D.U., Chapin, F.S., Ewel, J.J., Hector, A., Inchausti, P., Lavorel, S., Lawton,
J.H., Lodge, D.M., Loreau, M., Naeem, S., Schmid, B., Setälä, H., Symstad, A.J.,
Vandermeer, J., Wardle, D.A., 2005. Effects of biodiversity on ecosystem
functioning: a consensus of current knowledge. Ecol. Monogr. 75, 3–35.
Horn, S., Hanula, J.L., 2004. A Survey of Cavity-Nesting Bees and Wasps in Loblolly
Pine Stands of the Savannah River Site, Aiken County, South Carolina. J. Entomol.
Sci. 39, 464–469. https://doi.org/10.18474/0749-8004-39.3.464
Intergovernmental Science‐Policy Platform on Biodiversity and Ecosystem Services,
2016. Summary for policymakers of the assessment report of the Intergovernmental
Science‐Policy Platform on Biodiversity and Ecosystem Services on pollinators,
pollination and food production. Bonn, Germany.
Jenkins, D.A., Matthews, R.W., 2004. Cavity-nesting Hymenoptera in Disturbed Habitats
of Georgia and South Carolina: Nest Architecture and Seasonal Occurrence. J.
Kansas Entomol. Soc. 77, 203–214. https://doi.org/10.2317/0212.18a.1
Julier, H.E., Roulston, T.H., 2009. Wild Bee Abundance and Pollination Service in
Cultivated Pumpkins: Farm Management, Nesting Behavior and Landscape Effects.
J. Econ. Entomol. 102, 563–573. https://doi.org/10.1603/029.102.0214
Kearns, C.A., Inouye, D.W., Waser, N.M., 1998. Endangered Mutualisms: The
Conservation of Plant-Pollinator Interactions. Annu. Rev. Ecol. Syst. 29, 83–112.
https://doi.org/10.1146/annurev.ecolsys.29.1.83
King, J.R., Porter, S.D., 2005. Evaluation of Sampling Methods and Species Richness
Estimators for Ants in Upland Ecosystems in Florida. Environ. Entomol. 34, 1566–
79 1578. https://doi.org/10.1603/0046-225X-34.6.1566
Klatt, B.K., Holzschuh, A., Westphal, C., Clough, Y., Smit, I., Pawelzik, E., Tscharntke,
T., 2013. Bee pollination improves crop quality, shelf life and commercial value.
Proc. R. Soc. B Biol. Sci. 281, 20132440–20132440.
https://doi.org/10.1098/rspb.2013.2440
Kleijn, D., Winfree, R., Bartomeus, I., Carvalheiro, L.G., Henry, M., Isaacs, R., Klein,
A.-M., Kremen, C., M’Gonigle, L.K., Rader, R., Ricketts, T.H., Williams, N.M.,
Lee Adamson, N., Ascher, J.S., Báldi, A., Batáry, P., Benjamin, F., Biesmeijer, J.C.,
Blitzer, E.J., Bommarco, R., Brand, M.R., Bretagnolle, V., Button, L., Cariveau,
D.P., Chifflet, R., Colville, J.F., Danforth, B.N., Elle, E., Garratt, M.P.D., Herzog,
F., Holzschuh, A., Howlett, B.G., Jauker, F., Jha, S., Knop, E., Krewenka, K.M., Le
Féon, V., Mandelik, Y., May, E.A., Park, M.G., Pisanty, G., Reemer, M., Riedinger,
V., Rollin, O., Rundlöf, M., Sardiñas, H.S., Scheper, J., Sciligo, A.R., Smith, H.G.,
Steffan-Dewenter, I., Thorp, R., Tscharntke, T., Verhulst, J., Viana, B.F., Vaissière,
B.E., Veldtman, R., Ward, K.L., Westphal, C., Potts, S.G., 2015. Delivery of crop
pollination services is an insufficient argument for wild pollinator conservation. Nat.
Commun. 6, 7414. https://doi.org/10.1038/ncomms8414
Klein, A.-M., 2009. Nearby rainforest promotes coffee pollination by increasing spatio-
temporal stability in bee species richness. For. Ecol. Manage. 258, 1838–1845.
https://doi.org/10.1016/J.FORECO.2009.05.005
Klein, A.-M., Vaissière, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A.,
Kremen, C., Tscharntke, T., 2007. Importance of pollinators in changing landscapes
80 for world crops. Proc. R. Soc. B Biol. Sci. 274, 303–313.
https://doi.org/10.1098/rspb.2006.3721
Klein, A.-M., Vaissière, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A.,
Kremen, C., Tscharntke, T., 2006. Importance of pollinators in changing landscapes
for world crops. Proc. R. Soc. B Biol. Sci. 274, 303–313.
https://doi.org/10.1098/rspb.2006.3721
Kluser, Peduzzi, P., 2007. Global Pollinator Decline: A Literature Review. Geneva,
Switzerland.
Kremen, C., 2008. Crop pollination services from wild bees, in: James, R., Pitts-Singer,
T. (Eds.), Bee Pollination in Agricultural Ecosystems. Oxford University Press, pp.
8–26.
Kremen, C., Williams, N.M., Bugg, R.L., Fay, J.P., Thorp, R.W., 2004. The area
requirements of an ecosystem service: crop pollination by native bee communities in
California. Ecol. Lett. 7, 1109–1119. https://doi.org/10.1111/j.1461-
0248.2004.00662.x
Kremen, C., Williams, N.M., Thorp, R.W., 2002a. Crop pollination from native bees at
risk from agricultural intensification. Proc. Natl. Acad. Sci. 99, 16812–16816.
https://doi.org/10.1073/PNAS.262413599
Kremen, C., Williams, N.M., Thorp, R.W., 2002b. Crop pollination from native bees at
risk from agricultural intensification. Proc. Natl. Acad. Sci. 99, 16812–16816.
https://doi.org/10.1073/pnas.262413599
Larsen, T.H., Williams, N.M., Kremen, C., 2005. Extinction order and altered community
81 structure rapidly disrupt ecosystem functioning. Ecol. Lett. 8, 538–547.
https://doi.org/10.1111/j.1461-0248.2005.00749.x
Lee, K. V., Steinhauer, N., Rennich, K., Wilson, M.E., Tarpy, D.R., Caron, D.M., Rose,
R., Delaplane, K.S., Baylis, K., Lengerich, E.J., Pettis, J., Skinner, J.A., Wilkes, J.T.,
Sagili, R., vanEngelsdorp, D., Partnership, for the B.I., 2015. A national survey of
managed honey bee 2013–2014 annual colony losses in the USA. Apidologie 46,
292–305. https://doi.org/10.1007/s13592-015-0356-z
Mallinger, R.E., Gratton, C., 2015. Species richness of wild bees, but not the use of
managed honeybees, increases fruit set of a pollinator-dependent crop. J. Appl. Ecol.
52, 323–330. https://doi.org/10.1111/1365-2664.12377
Matteson, K.C., Ascher, J.S., Langellotto, G.A., 2008. Bee Richness and Abundance in
New York City Urban Gardens. Ann. Entomol. Soc. Am. 101, 140–150.
https://doi.org/10.1603/0013-8746(2008)101[140:braain]2.0.co;2
McCall, C., Primack, R.B., 1992. Influence of flower characteristics, weather, time of
day, and season on insect visitation rates in three plant communities. Am. J. Bot. 79,
434–442. https://doi.org/10.1002/j.1537-2197.1992.tb14571.x
Mcgregor, S.E., 1976. Insect Pollination Of Cultivated Crop Plants. Washington, DC.
Michener, C.D., 2007. The bees of the world, 2nd ed. Johns Hopkins University Press,
Baltimore.
Michener, C.D., 2000. The bees of the world, 1st ed. Johns Hopkins University Press,
Baltimore.
Michener, C.D., 1979. Biogeography of the Bees. Ann. Missouri Bot. Gard. 66, 277.
82 https://doi.org/10.2307/2398833
Morandin, L.A., Kremen, C., 2013. Hedgerow restoration promotes pollinator
populations and exports native bees to adjacent fields. Ecol. Appl. 23, 829–839.
https://doi.org/10.1890/12-1051.1
Morse, R.A., Calderone, N.W., 2000. The value of honey bees as pollinators of US crops
in 2000. Bee Cult. 128, 1–15.
Mueller, U.G., 1996. Life History and Social Evolution of the Primitively Eusocial Bee
Augochlorella striata (Hymenoptera: Halictidae). J. Kansas Entomol. Soc.
https://doi.org/10.2307/25085710
National Research Council (U.S.), 2007. Committee on the Status of Pollinators in North
America. National Academies Press.
Owen, J., Gilbert, F.S., 1989. On the Abundance of Hoverflies (Syrphidae). Oikos 55,
183. https://doi.org/10.2307/3565422
Packer, L., 1990. Solitary and eusocial nests in a population of Augochlorella striata
(Provancher) (Hymenoptera; Halictidae) at the northern edge of its range. Behav.
Ecol. Sociobiol. 27, 339–344. https://doi.org/10.1007/BF00164004
Potts, S., Biesmeijer, J., Kremen, C., Neumann, P., Schweiger, O., Kunin, W., 2010.
Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25, 345–
353. https://doi.org/10.1016/J.TREE.2010.01.007
Primack, R., Primack, R.B., 1978. Plant phenology in Botanical Gardens View project
Tree Demographics in Malaysian Rainforest View project variability in New
Zealand montane and alpine pollinator assemblages, NEW ZEALAND JOURNAL
83 OF ECOLOGY.
Pywell, R.F., Warman, E.A., Hulmes, L., Hulmes, S., Nuttall, P., Sparks, T.H., Critchley,
C.N.R., Sherwood, A., 2006. Effectiveness of new agri-environment schemes in
providing foraging resources for bumblebees in intensively farmed landscapes. Biol.
Conserv. 129, 192–206. https://doi.org/10.1016/J.BIOCON.2005.10.034
Rader, R., Bartomeus, I., Garibaldi, L.A., Garratt, M.P.D., Howlett, B.G., Winfree, R.,
Cunningham, S.A., Mayfield, M.M., Arthur, A.D., Andersson, G.K.S., Bommarco,
R., Brittain, C., Carvalheiro, L.G., Chacoff, N.P., Entling, M.H., Foully, B., Freitas,
B.M., Gemmill-Herren, B., Ghazoul, J., Griffin, S.R., Gross, C.L., Herbertsson, L.,
Herzog, F., Hipólito, J., Jaggar, S., Jauker, F., Klein, A.-M., Kleijn, D., Krishnan, S.,
Lemos, C.Q., Lindström, S.A.M., Mandelik, Y., Monteiro, V.M., Nelson, W.,
Nilsson, L., Pattemore, D.E., Pereira, N. de O., Pisanty, G., Potts, S.G., Reemer, M.,
Rundlöf, M., Sheffield, C.S., Scheper, J., Schüepp, C., Smith, H.G., Stanley, D.A.,
Stout, J.C., Szentgyörgyi, H., Taki, H., Vergara, C.H., Viana, B.F., Woyciechowski,
M., 2016. Non-bee insects are important contributors to global crop pollination.
Proc. Natl. Acad. Sci. 113, 146–151. https://doi.org/10.1073/PNAS.1517092112
Rader, R., Reilly, J., Bartomeus, I., Winfree, R., 2013. Native bees buffer the negative
impact of climate warming on honey bee pollination of watermelon crops. Glob.
Chang. Biol. 19, 3103–3110. https://doi.org/10.1111/gcb.12264
Ramsden, M.W., Menéndez, R., Leather, S.R., Wäckers, F., 2015. Optimizing field
margins for biocontrol services: The relative role of aphid abundance, annual floral
resources, and overwinter habitat in enhancing aphid natural enemies. Agric.
84 Ecosyst. Environ. 199, 94–104. https://doi.org/10.1016/J.AGEE.2014.08.024
Rightmyer, M.G., 2008. A review of the cleptoparasitic bee genus Triepeolus
(Hymenoptera: Apidae).-Part I. Zootaxa 1710, 1–170.
Roulston, T.H., Goodell, K., 2011. The Role of Resources and Risks in Regulating Wild
Bee Populations. Annu. Rev. Entomol. 56, 293–312.
https://doi.org/10.1146/annurev-ento-120709-144802
Rozen, J.G., 2001. A Taxonomic Key to Mature Larvae of Cleptoparasitic Bees
(Hymenoptera: Apoidea). Am. Museum Novit. 3309, 1–28.
https://doi.org/10.1206/0003-0082(2001)309<0001:ATKTML>2.0.CO;2
Russo, L., Park, M., Gibbs, J., Danforth, B., 2015. The challenge of accurately
documenting bee species richness in agroecosystems: bee diversity in eastern apple
orchards. Ecol. Evol. 5, 3531–3540. https://doi.org/10.1002/ece3.1582
Rust, R.W., 1980. The Biology of Ptilothrix bombiformis (Hymenoptera:
Anthophoridae). J. Kansas Entomol. Soc. https://doi.org/10.2307/25084048
Sanders, H.L., 1968. Marine Benthic Diversity: A Comparative Study. Am. Nat. 102,
243–282. https://doi.org/10.1086/282541
Sardiñas, H., Kremen, C., 2015. Pollination services from field-scale agricultural
diversification may be context-dependent. Agric. Ecosyst. Environ. 17–25.
Sardiñas, H.S., Kremen, C., 2015. Pollination services from field-scale agricultural
diversification may be context-dependent. Agric. Ecosyst. Environ. 207, 17–25.
https://doi.org/10.1016/J.AGEE.2015.03.020
Sheffield, C.S., Kevan, P.G., Smith, R.F., 2003. Bee Species of Nova Scotia, Canada,
85 with New Records and Notes on Bionomics and Floral Relations (Hymenoptera:
Apoidea). J. Kansas Entomol. Soc. https://doi.org/10.2307/25086122
Sheffield, C.S., Pindar, A., Packer, L., Kevan, P.G., 2013a. The potential of
cleptoparasitic bees as indicator taxa for assessing bee communities. Apidologie 44,
501–510. https://doi.org/10.1007/s13592-013-0200-2
Sheffield, C.S., Pindar, A., Packer, L., Kevan, P.G., 2013b. The potential of
cleptoparasitic bees as indicator taxa for assessing bee communities. Apidologie 44,
501–510. https://doi.org/10.1007/s13592-013-0200-2
Sheffield CS, Kevan PG, Pindar A, Packer L, 2013. Bee (Hymenoptera: Apoidea)
diversity within apple orchards and old fields in the Annapolis Valley, Nova Scotia,
Canada. Can. Entomol. 145, 94–114.
Shepherd, M., Ross, E.S., 2003. Pollinator conservation handbook. Xerces Society in
association with Bee Works.
Simberloff, D., 1978. Use of rarefaction and related methods in ecology, in: Dickson,
K.L., Garins, Jr., J., Livingston, R.J. (Eds.), Biological Data in Water Pollution
Assessment: Quantitative and Statistical Analysis. American Society for Testing and
Materials, Easton, MD, pp. 150–165.
South Carolina Department of Agriculture 2019., 2019. Watermelon production [WWW
Document]. URL http://agriculture.sc.gov/resources/agriculture-organizations/south-
carolina-watermelon/production/
Staley, J.T., Sparks, T.H., Croxton, P.J., Baldock, K.C.R., Heard, M.S., Hulmes, S.,
Hulmes, L., Peyton, J., Amy, S.R., Pywell, R.F., 2012. Long-term effects of
86 hedgerow management policies on resource provision for wildlife. Biol. Conserv.
145, 24–29. https://doi.org/10.1016/J.BIOCON.2011.09.006
Stanghellini, M.S., Ambrose, J.T., Schultheis, J.R., 2002. Diurnal activity, floral
visitation and pollen deposition by honey bees and bumble bees on field-grown
cucumber and watermelon. J. Apic. Res. 41, 27–34.
https://doi.org/10.1080/00218839.2002.11101065
Steffan-Dewenter, I., Potts, S.G., Packer, L., 2005. Pollinator diversity and crop
pollination services are at risk. Trends Ecol. Evol. 20, 651-2; author reply 652-3.
https://doi.org/10.1016/j.tree.2005.09.004
Stockhammer, K.A., 1966. Nesting Habits and Life Cycle of a Sweat Bee, Augochlora
pura (Hymenoptera: Halictidae). J. Kansas Entomol. Soc.
https://doi.org/10.2307/25083506
Tilman, D., Fargione, J., Wolff, B., D’Antonio, C., Dobson, A., Howarth, R., Schindler,
D., Schlesinger, W.H., Simberloff, D., Swackhamer, D., 2001a. Forecasting
agriculturally driven global environmental change. Science 292, 281–4.
https://doi.org/10.1126/science.1057544
Tilman, D., Fargione, J., Wolff, B., D’Antonio, C., Dobson, A., Howarth, R., Schindler,
D., Schlesinger, W.H., Simberloff, D., Swackhamer, D., 2001b. Forecasting
agriculturally driven global environmental change. Science 292, 281–4.
https://doi.org/10.1126/science.1057544
UGA, E., 2017. Commercial Watermelon Production.
Vázquez, D.P., Morris, W.F., Jordano, P., 2005. Interaction frequency as a surrogate for
87 the total effect of animal mutualists on plants. Ecol. Lett. 8, 1088–1094.
https://doi.org/10.1111/j.1461-0248.2005.00810.x
Waser, N.M., 1986. Flower Constancy: Definition, Cause, and Measurement. Am. Soc.
Nat. 127, 593–603.
Wcislo, W.T., Engel, M.S., 1996. Social Behavior and Nest Architecture of Nomiine
Bees (Hymenoptera: Halictidae; Nomiinae). J. Kansas Entomol. Soc.
https://doi.org/10.2307/25085713
Williams, N.M., Minckley, R.L., Silveira, F.A., 2001. Variation in native bee faunas and
its implications for detecting community changes. Conserv. Ecol. 5.
Williams, P.H., Osborne, J.L., 2009. Bumblebee vulnerability and conservation world-
wide. Apidologie 40, 367–387. https://doi.org/10.1051/apido/2009025
Williams, P.H., Thorp, R.W., Richardson, L.L., Colla, S.R., 2014. Bumble bees of North
America: an identification guide. Princeton University Press.
Winfree, R., 2010. The conservation and restoration of wild bees. Ann. N. Y. Acad. Sci.
1195, 169–197. https://doi.org/10.1111/j.1749-6632.2010.05449.x
Winfree, R., Aguilar, R., Vázquez, D.P., LeBuhn, G., Aizen, M.A., 2009. A meta-
analysis of bees’ responses to anthropogenic disturbance. Ecology 90, 2068–2076.
https://doi.org/10.1890/08-1245.1
Winfree, R., Gross, B.J., Kremen, C., 2011. Valuing pollination services to agriculture.
Ecol. Econ. 71, 80–88. https://doi.org/10.1016/J.ECOLECON.2011.08.001
Winfree, R., Williams, N.M., Gaines, H., Ascher, J.S., Kremen, C., 2008. Wild bee
pollinators provide the majority of crop visitation across land-use gradients in New
88 Jersey and Pennsylvania, USA. J. Appl. Ecol. 45, 793–802.
https://doi.org/10.1111/j.1365-2664.2007.01418.x
Winfree, R., Williams, N.M., Gaines, H., Ascher, J.S., Kremen, C., 2007. Wild bee
pollinators provide the majority of crop visitation across land-use gradients in New
Jersey and Pennsylvania, USA. J. Appl. Ecol. 45, 793–802.
https://doi.org/10.1111/j.1365-2664.2007.01418.x
89 Table 2.1 Number of sampling events by site, year, specimens collected, and species richness (S)
Site name County Treatment Type #Sampling events #Specimens S
2015 B3 Charleston n/a 12 234 25 2016 C.A2 Charleston Control 7 28 6 C.OLAR Bamberg Control 2 67 13 C.F9 Charleston Control 7 52 16 T.11E Charleston Treatment 7 64 17 T. B3 Charleston Treatment 11 140 31 T.EREC Barnwell Treatment 4 101 19 2017
C.3D Charleston Control 5 50 17 C.4K Charleston Control 5 50 21 C.B9 Charleston Control 3 31 14 C.EREC Barnwell Control 3 21 15 C.ROSE Charleston Control 1 14 10 T.4E Charleston Treatment 8 87 25 T.4G Charleston Treatment 9 212 33 T.B1 Charleston Treatment 10 184 36 T.EREC Barnwell Treatment 5 204 29 T.ROSE Charleston Treatment 2 40 12 2018
W.4G Charleston Within 14 254 24 W.B1 Charleston Within 11 211 31 W.B11 Charleston Within 13 218 35 W.EREC Barnwell Within 2 95 17 N.D8 Charleston Near 5 16 18 N.F9 Charleston Near 7 44 25 N.FREE Charleston Near 3 49 15 N.ROSE1 Charleston Near 3 62 22 N.ROSE2 Charleston Near 3 71 34 N.EREC Barnwell Near 1 26 9
90 Table 2.2. Citrullus lanatus visitors by number of individuals collected per year, number of sites where they were collected/observed on C.lanatus, whether they were collected/observed on wildflower species ( C.sul=Cosmos sulphureus, C.tin=Coreopsis tinctoria, G.pul=Gaillardia pulchella, V.hast=Verbena hastata, Z.eleg=Zinnia elegans) , and what bee guild they belong to if a bee (SOL=solitary ground nesters, SOC=social ground nesters, BOM=bumble bees, HB=honey bee, CN=cavity nesters, CLE=cleptoparasites)
Genus species Author 2018 2017 2016 2015 #Sites C.sul C.tin G.pul V.hast Z.eleg Guild
Hymenoptera
Agapostemon splendens Lepeletier 21 40 49 7 20 X X X X X SOL Augochlora pura Say 0 0 1 0 1 CN Augochlorella aurata Smith 48 21 1 19 9 X SOC 1 Augochloropsis metallica fulgida Fabricius 0 0 1 0 1 SOL 2 Augochloropsis sumptuosa Smith 0 0 3 0 1 SOL 2 Apis mellifera Linnaeus * na na na na 20 X X X X HB Bombus fraternus Smith 6 8 13 3 10 X X X X X BOM Bombus griseocollis DeGeer 7 3 21 0 9 X X X X X BOM Bombus impatiens Cresson 43 24 34 43 19 X X X X X BOM Bombus pensylvanicus DeGeer 6 8 4 2 11 X X X X BOM Campsomeris sp. 4 0 1 0 4 X X X - Ceratina floridana Mitchell 9 2 0 0 6 CN Coelioxys sayi Robertson 0 0 1 0 1 X X X CLE
91 Colletes nudus Robertson 1 0 0 0 1 X SOL Halictus poeyi Lepeletier 35 85 25 0 13 X X X X X SOC 3 Halictus rubicundus Christ 0 0 2 0 1 SOC 3 Hylaeus ornatus Mitchell 0 3 0 0 1 CN Lasioglossum callidum Sandhouse 167 202 96 52 18 X X X X X SOC Lasioglossum creberrimum Smith 2 1 8 3 4 X SOC Lasioglossum floridanum Robertson 1 0 0 0 1 SOC Lasioglossum imitatum Smith 2 0 1 1 3 SOC Lasioglossum leviense Mitchell 4 0 0 0 1 SOC Lasioglossum longifrons Baker 6 7 1 0 5 X X X X SOC Lasioglossum lustrans Cockerell 0 1 0 1 2 SOL Lasioglossum nelumbonis Robertson 3 0 0 0 2 SOL Lasioglossum nymphale Smith 1 0 2 0 3 SOC Lasioglossum pectoral Smith 3 1 0 0 4 SOL Lasioglossum pilosum Smith 2 1 4 0 4 SOC Lasioglossum puteulanum Gibbs 23 8 10 1 14 SOC Lasioglossum reticulatum Robertson 9 2 0 3 5 SOC Lasioglossum sp. 8 12 5 0 11 X X X X ? Lasioglossum tamiamense Mitchell 40 14 0 0 12 X X X SOC
92 Lasioglossum tegulare Robertson 18 0 0 0 7 SOC Lasioglossum trigeminum Gibbs 0 2 5 0 6 X SOC Megachile mendica Cresson 22 59 31 42 14 X X X X X CN Megachile petulans Cresson 1 0 2 0 2 X X X X CN Megachile pseudobrevis Mitchell 0 1 0 0 1 X X CN Megachile texana Cresson 3 0 0 0 1 X X X CN Megachile xylocopoides Smith 0 0 1 2 2 X X X CN Melissodes bimaculata Lepeletier 27 15 20 22 13 X X X X X SOL Melissodes communis Cresson 25 45 21 5 22 X X X X SOL Melissodes comptoides Robertson 5 2 0 0 4 X X SOL Melissodes tepanaca Cresson 0 1 3 0 3 SOL Melissodes trinodis Robertson 0 1 1 0 2 X SOL Melitoma taurea Say 1 0 1 0 2 SOL Nomada fervida Smith 0 1 0 0 1 X X X CLE Nomada vegana Cockerell 0 1 0 0 1 X CLE Sphecodes sp. 1 2 0 1 4 X CLE Triepeolus concavus Cresson 0 0 1 0 1 X X X X CLE Triepeolus simplex Robertson 1 0 0 0 1 X CLE Xenoglossa strenua Cresson 0 1 0 0 1 SOL
93 Xylocopa micans Lepeletier 18 7 4 1 13 X X CN Xylocopa virginica Linnaeus 12 8 7 2 16 X X X X X CN Diptera
Toxomerus sp. 11 3 0 0 6 X - Palpada sp. 9 9 1 0 11 X X X X X - Lepidoptera
Agraulis vanillae Linnaeus* na na na na 2 X X - Hesperiidae* na na na na 6 X - Pieris rapae Linnaeus * na na na na 1 - Urbanus proteus Linnaeus * 0 0 0 0 2 X -
*Indicates species that were observed only, not collected 1 Species occasionally exhibits solitary or semi-social behavior (Packer 1990, Mueller 1996, Gibbs 2017) 2 Species exhibit solitary, communal (Wolf and Ascher 2009, Goldstein and Ascher 2016) and possibly semi-social behavior (Gibbs 2017) 3 Facultatively eusocial—intraspecific variation in social behavior according to environmental conditions, primitively eusocial in temperate conditions, communal in tropics (Packer and Knerer 1996) Note: Lasioglossum (Dialictus) is thought to primarily consist of primitively eusocial ground nesters, but the species in this subgenus vary from solitary to primitively eusocial (Jason Gibbs, personal communication, Michener 1974). Some species (i.e. L.callidum, L.creberrimum), have not been studied or were possibly studied by Charles Michener (Jason Gibbs personal communication).
94 70 59 60 52 50
40 34 31 30 29 28 30 27 26 22 20 # Pollinator # Species
10
0 Citrullus lanatus Coreopsis tinctoria Cosmos sulphureus Gaillardia pulchella Zinnia elegans
All insect visitors Apoidea visitors
Fig 2.1. Number of pollinator species collected in 2015-2018 visiting focal species (Citrullus lanatus ) and wildflower species
95 Table 2.3. List of wildflower ( C.sul=Cosmos sulphureus, C.tin=Coreopsis tinctoria, G.pul=Gaillardia pulchella, V.hast=Verbena hastata, Z.eleg=Zinnia elegans) visitors by number of sites where they were collected/ observed, total number of individuals collected over four years per floral species , whether they were also collected/observed on Citrullus lanatus.(C.lan) , and what bee guild they belong to if a bee (SOL=solitary ground nesters, SOC=social ground nesters, BOM=bumble bees, HB= honey bee, CN=cavity nesters, CLE=cleptoparasites)
Genus species Author #Sites C.sul C.tin G,pul V.hast Z.eleg C.lan Guild
Hymenoptera
Agapostemon splendens Lepeletier 11 3 2 10 2 1 x SOL Apis mellifera Linnaeus 20 x x x x HB Augochlorella aurata Smith 9 0 3 0 0 0 x SOC 1 Bombus fraternus Smith 13 11 3 2 5 6 x BOM Bombus griseocollis DeGeer 14 11 1 5 2 14 x BOM Bombus impatiens Cresson 20 5 2 3 0 8 x BOM Bombus pensylvanicus DeGeer 13 11 0 6 2 18 x BOM Campsomeris sp. 7 0 1 1 1 0 x - Coelioxys sayi Robertson 4 3 0 5 1 0 x CLE Colletes nudus Robertson 2 1 0 0 0 0 x SOL Dieunomia heteropoda Say 7 25 72 27 0 3 SOL Halictus poeyi Lepeletier 17 15 34 87 1 38 x SOC 2 Lasioglossum callidum Sandhouse 18 1 46 59 5 105 x SOC
96 Lasioglossum creberrimum Smith 4 0 5 0 0 0 x SOC Lasioglossum longifrons Baker 5 4 2 1 0 2 x SOC Lasioglossum sp. 12 0 3 3 1 3 x ? Lasioglossum tamiamense Mitchell 13 0 27 3 0 1 x SOC Lasioglossum trigeminum Gibbs 6 0 1 0 0 0 x SOC Megachile albitarsis Cresson 1 0 1 0 0 0 CN Megachile campanulae Robertson 1 1 0 0 0 0 CN Megachile mendica Cresson 17 30 5 44 8 2 x CN Megachile petulans Cresson 7 0 7 9 1 5 x CN Megachile pseudobrevis Mitchell 3 0 0 1 1 0 x CN Megachile sculpturalis Smith 1 0 0 0 1 0 CN Megachile sp. 12 0 1 5 1 1 CN Megachile texana Cresson 5 0 0 2 2 1 x CN Megachile xylocopoides Smith 9 5 5 0 10 0 x CN Melissodes bimaculata Lepeletier 14 11 2 1 1 3 x SOL Melissodes communis Cresson 22 8 3 11 0 4 x SOL Melissodes comptoides Robertson 4 1 0 2 0 0 x SOL Melissodes subillata LaBerge 1 0 1 0 0 0 SOL Melissodes trinodis Robertson 2 0 0 1 0 0 x SOL
97 Nomada fervida Smith 2 1 0 1 1 0 x CLE Nomada vegana Cockerell 1 0 0 1 0 0 x CLE Nomia nortoni Cresson 1 0 1 0 0 0 SOL 3 Ptilothrix bombiformis Cresson 1 0 0 0 0 1 SOL Scolia sp. 1 0 1 0 0 0 - Sphecodes sp. 4 0 2 0 0 0 x CLE Svastra aegis LaBerge 5 14 5 17 0 2 SOL Svastra obliqua Say 7 7 5 35 0 15 SOL Svastra petulca Cresson 5 0 6 6 0 1 SOL Triepeolus concavus Cresson 7 5 1 6 0 1 x CLE Triepeolus lunatus Say 2 6 0 8 1 0 CLE Triepeolus remigatus Fabricius 1 9 0 0 0 0 CLE Triepeolus simplex Robertson 3 0 0 3 0 0 x CLE Xylocopa micans Lepeletier 13 5 0 0 4 0 x CN Xylocopa virginica Linnaeus 18 2 2 0 1 3 x CN
Diptera
Palpada sp. 12 4 5 6 4 8 x - Toxomerus sp. 6 0 2 0 0 0 x -
98
Lepidoptera
Agraulis vanillae Linnaeus * 5 x x x - Danaus plexippus Linnaeus * 1 0 0 0 0 x - Epargyreus clarus Cramer * 2 x x - Euptoieta claudia Cramer * 1 x - Heliconius charithonia Linnaeus * 1 x - Junonia coenia Hubner * 1 x - Papilio polyxenes asterius Stoll * 3 x - Papilio glaucus Hodges * 4 x - Papilio palamedes Drury * 4 x x x - Phoebus sennae Linnaeus * 1 x - Urbanus proteus* Linnaeus 2 x x -
*Indicates species that were observed only, not collected 1 Species occasionally exhibits solitary or semi-social behavior (Packer 1990, Mueller 1996, Gibbs 2017) 2 Facultatively eusocial—intraspecific variation in social behavior according to environmental conditions, primitively eusocial in temperate conditions, communal in tropics (Packer and Knerer 1996) 3 Possibly communal, Park 1928
99 35 31 A 30
s 25 e 19 17 18 ec i 20 16 16
p 15 13 S
15 # 10 6 5 0 C.A2 C.F9 C.OLAR T.11E T.B3 T.EREC
40 36 33 B 29 30 25
s 23 e 20 20 20 17 15 15 14 14 12 10 10 #Sp ec i 10
0 USDA 1 USDA 2 CREC EREC Rosebank
40 35 34 C 31 %!
s 24 25 e 21 21 22 19 20 ec i 17 18 p 20 15 15 15 S 11 # 8 9 9 6
0 W.4G W.B1 W.B11 W.EREC N.F9 N.D8 N.FREE N.EREC N.ROSE1 N.ROSE2 C.lanatus pollinators Control All pollinators C.lanatus pollinators
Figure 2.2. Total number of pollinator species including observed and collected species at control fields (grey) and treatment fields (black and white) in 2016 (A), 2017 (B) and 2018 (C). In 2016, fields are referred to by field name preceded by treatment type (C- control, T-Treatment). In 2017, fields are referred to by name only because each site was a block consisting of both treatment and control fields. In 2018, fields are referred to by name preceded by treatment type (W-wildflower within, N-wildflower nearby).
100 Table 2.4. Species and number of specimens collected with bee bowls in 2016
Genus species (author) #Specimens Lasioglossum longifrons (Baker) 116 Lasioglossum callidum (Sandhouse) 56 Melissodes communis (Cresson) 24 Melissodes bimaculata (Lepeletier) 21 Lasioglossum puteulanum (Gibbs) 18 Megachile mendica (Cresson) 14 Lasioglossum creberrimum (Smith) 8 Lasioglossum reticulatum (Robertson) 7 Apis mellifera (Linnaeus) 6 Xylocopa virginica (Linnaeus) 5 Agapostemon splendens (Lepeletier) 3 Augochlorella aurata (Smith) 4 Bombus griseocollis (DeGeer) 2 Halictus poeyi (Lepeletier) 2 Hylaeus ornatus (Mitchell) 2 Melissodes tepanaca (Cresson) 2 Lasioglossum imitatum (Smith) 1 Melitoma taurea (Say) 1 Ptilothrix bombiformis (Cresson) 1 Xylocopa micans (Lepeletier) 1
101 Table 2.5 Jaccard similarity matrix of pollinator community composition for all fields by year. In 2018, “W” before the field name indicates those with wildflowers within the field, and “N” before the name indicates field with wildflowers nearby. In 2016 and 2017, “C” before the field name indicates control fields (no wildflowers), and “T” before the name indicates treatment fields (with wildflowers).
2018 N.EREC N.D8 N.F9 N.FREE N.ROSE1 N.ROSE2 W.4G W.EREC W.B1 W.B11 N.EREC - 0 0.18 0.2 0.22 0.14 0.1 0.25 0.19 0.16
N.D8 0 - 0.33 0.11 0.14 0.13 0.26 0.05 0.22 0.19 N.F9 0.18 0.33 - 0.52 0.44 0.44 0.38 0.21 0.61 0.43 N.FREE 0.2 0.11 0.52 - 0.33 0.36 0.17 0.18 0.32 0.31 N.ROSE1 0.22 0.14 0.44 0.33 - 0.27 0.23 0.2 0.32 0.28 N.ROSE2 0.14 0.13 0.44 0.36 0.27 - 0.2 0.25 0.46 0.4 W.4G 0.1 0.26 0.38 0.17 0.23 0.2 - 0.2 0.37 0.39 W.EREC 0.25 0.05 0.21 0.18 0.2 0.25 0.2 - 0.26 0.22 W.B1 0.19 0.22 0.61 0.32 0.32 0.46 0.37 0.26 - 0.67 W.B11 0.16 0.19 0.43 0.31 0.28 0.4 0.39 0.22 0.67 -
102 2017 C.3D C.4K C.B9 C.EREC C.ROSE T.4E T.4G T.B1 T.EREC T.ROSE C.3D - 0.33 0.33 0.29 0.25 0.35 0.35 0.26 0.40 0.30 C.4K 0.33 - 0.29 0.25 0.21 0.21 0.32 0.24 0.21 0.28 C.B9 0.33 0.29 - 0.33 0.08 0.14 0.21 0.29 0.19 0.27 C.EREC 0.29 0.25 0.33 - 0.15 0.17 0.24 0.26 0.31 0.25 C.ROSE 0.25 0.21 0.08 0.15 - 0.20 0.12 0.13 0.29 0.13 T.4E 0.35 0.21 0.14 0.17 0.20 - 0.48 0.41 0.36 0.56 T.4G 0.35 0.32 0.21 0.24 0.12 0.48 - 0.40 0.26 0.59 T.B1 0.26 0.24 0.29 0.26 0.13 0.41 0.40 - 0.23 0.37 T.EREC 0.40 0.21 0.19 0.31 0.29 0.36 0.26 0.23 - 0.32 T.ROSE 0.30 0.28 0.27 0.25 0.13 0.56 0.59 0.37 0.32 -
2016 T.11E T.B3 T.EREC C.A2 C.F9 C.OLAR T.11E - 0.36 0.33 0.29 0.41 0.38 T.B3 0.36 - 0.21 0.22 0.42 0.25 T.EREC 0.33 0.21 - 0.13 0.35 0.47 C.A2 0.29 0.22 0.13 - 0.31 0.19 C.F9 0.41 0.42 0.35 0.31 - 0.33
C.OLAR 0.38 0.25 0.47 0.19 0.33 -
103 Table 2.6 Means and standard error of Jaccard similarity indices of pollinator community composition by year between watermelon fields with (treatment) and without (control) wildflowers in 2016 and 2017, and fields with wildflowers near the field and within the field in 2018. 2016 2017 2018
Mean SE Mean SE Mean SE Control 0.28 0.04 0.40 0.03 Within field 0.35 0.07 Treatment 0.30 0.04 0.25 0.03 Near field 0.25 0.04
Table 2.7 ANOVA test for difference between Jaccard similarity means in 2016 (control fields mean similarity index vs. treatment fields mean similarity index), 2017 (same as 2016), 2018 (wildflowers within fields mean similarity index vs. wildflowers near field mean similarity index). 2016 2017 2018 df F p df F p df F p 1,4 0.14 0.73 1,18 10.19 0.005* 1,19 1.72 0.21
105 Table 2.8 Jaccard similarity of pollinator community composition between paired watermelon fields in 2017. Each pair/block consisted of a control field (without wildflowers) and a treatment field (with wildflowers).
Field name Similarity index USDA 1 0.35 USDA 2 0.32 EREC 0.26 ROSE 0.29 CREC 0.27
106 Table 2.9 Jaccard similarity of pollinator community composition for watermelon fields studied multiple years
Field name Similarity index Years sampled 4G 0.36 2017, 2018 B1 0.48 2017, 2018 B3 0.44 2015, 2016 EREC CTL 0.23 2016, 2017, 2018 EREC WF 0.46 2016, 2017, 2018 F9 0.57 2016, 2018 ROSE WF 0.32 2017, 2018
107
Figure 2.3 . Species accumulation curve for all pollinator species using all sampling events (167). Species were collected with aerial nets at 28 watermelon fields in South Carolina from 2015-2018. The two outer lines represent upper and lower 95% confidence intervals.
108
Figure 2.4. Individual rarefaction curve for 28 sites where pollinators were collected from watermelon fields for four years. Sites with collections in multiple years are considered separate sites. Lines labelled beginning with “C” indicate control sites, “T” indicates treatment sites, “WIN” indicates fields with wildflowers within the field, and “NEAR” indicates fields with wildflowers nearby.
109
A
B
C
Figure 2.5. Individual rarefaction curves of all species collected in a) 2016 b) 2017 and c) 2018. “C” before site names indicate control sites and “T” indicates treatment fields. “NEAR” before site names indicates sites with wildflowers nearby, and “WIN” indicates sites with wildflowers within the field. 95% confidence intervals are represented. If the observed value falls within the confidence interval, then hypothesis that the richness of the smaller sample, based on all n individuals, does not differ from the richness of a subsample of size n* from the larger sample cannot be rejected at P≤0.05.
110 Supplementary information
Table 2.10 Wildflower species in 2016 treatment fields.
1. Scarlet Flax – Linum grandiflorum rubrum 2. Catch Fly – Silene armerla 3. Annual Baby’s Breath – Gypsophila elegans 4. Cornflower (Bachelor’s button) – Centaurea cyanus 5. Annual Gaillardia (Indian blanket) – Gaillardia pulchellia 6. Bachelor’s Button Tall mixed/Cornflower – Centaurea cynnus – Tall mixed 7. Cosmos – Cosmos bipinnatus 8. Sulphur Cosmos – Cosmos sulphureus 9. Plains Coreopsis – Coreopsis tinctoria 10. Swe et al. yssum – Lobularia maritima 11. Black eyed Susan, coastal plain NC Ecotype. Rudbeckia hirta 12. Spurred Snapdragon (Northern Lights) – Linaria maroccana 13. Annual Phlox – Phlox drummondii
111 CHAPTER 3
FORAGING BEHAVIOR OF WATERMELON POLLINATORS
Abstract—Providing additional floral resources in agricultural areas has been shown to facilitate crop pollination and improve fruit yields by attracting and maintaining a diverse native pollinator community in agricultural areas that are devoid of food resources outside of the crop blooming period. In this study I investigated two aspects of pollinator effectiveness that are not frequently included in the context of co-flowering species in agricultural systems: (1) flower handling time (the duration of each visit by a pollinator) and (2) floral constancy (a behavior in which a pollinator visits the same floral species in sequence even though other species are available). In watermelon fields in South
Carolina, I found that most watermelon pollinators exhibited floral constancy when observed on watermelon and co-flowering wildflower or weed species. However, bumble bees ( Bombus spp.) exhibited the highest rates of floral inconstancy with 42% of individuals moving between floral species in a foraging sequence on watermelon and
32% on wildflowers. In addition, large bees ( Bombus spp. and Xylocopa virginica ) and medium bees ( Melissodes spp., Megachile spp.) spent the least time foraging per flower while the smallest native bees ( Lasioglossum spp.) had the longest flower handling time.
Small bees, despite their low pollen deposition rates and long flower handling time, had high visitation frequencies in these watermelon fields in a previous study (chapter 1) and exhibited floral constancy. Thus, they probably play an important role in pollinating watermelon in this system. Large bees and medium bees are likely the most important pollinators of watermelon in my system, given their low flower handling time, high
112 visitation frequency (chapter 1) and high pollen deposition rates although bumble bees exhibited some floral inconstancy. The differences I observed in foraging behavior in watermelon bee pollinators likely contribute to pollinator niche complementarity, creating a more resilient and robust pollinator community.
INTRODUCTION
For effective pollination to occur, a complex set of factors are at play at different parts of the overall pollination process and are dependent on the varying life histories of plants and their pollinators (Willcox et al., 2017). Landscape and regional factors also impact pollinators through an array of environmental conditions, especially the availability of nesting and food resources (Andersson et al., 2014; Carvalheiro et al.,
2011; Kennedy et al., 2013). Currently, the most common way to assess pollination effectiveness is through combining pollinator foraging behavior, visitation rate and per visit pollen deposition to quantify pollinator performance (Willcox et al., 2017).
Visitation rates are cited as the most important factor determining a pollinator’s effectiveness (Morris, 2015; Vázquez et al., 2005). Others acknowledge that specific behaviors and interactions when on the flower (Brown and Mitchell, 2001; Flanagan et al., 2009; Wallace et al., 2002) and contribution to the plant’s female reproductive success ((Ne’eman et al., 2010) might be equally important factors. Whether individuals have pollen accessible on their body as they move between flowers (not stored in a pollen corbicula in the case of honey bees and bumble bees) and that this pollen comes into contact with the stigmatic surface of the flower will impact the pollination success
(Bosch and Blas, 1994; Wallace et al., 2002). In canola pollination, solitary bees showed
113 the greatest likelihood of contacting the stigma with their bodies because they spent more time on individual flowers and tended to collect pollen rather than nectar compared to honey bees which foraged for nectar (Woodcock et al., 2013). In macadamia nut pollination, stingless bees ( Trigona carbonaria ) are probably more effective pollinators than honey bees because they consistently come into direct contact with the stigma, tend to collect pollen while honey bees tend to collect nectar, and climb the styles to access the stigma while honey bees hover over the styles (Heard 1994). Grooming behavior and frequency and scopa (pollen collecting hairs) location and structure all contribute to the likelihood of transferring pollen onto the stigma (Flanagan et al 2009). Additional factors include pollinator morphology (Herrera, 1987), duration of individual visits (Young and
Stanton, 1990), and the proportion of conspecific and heterospecific pollen in the pollen load (Brown and Mitchell, 2001; Karron et al., 2006). Body size can affect various foraging capabilities such as the pollen load carried, tongue length which affects accessibility to nectar, and the relative size of the animal’s body and floral reproductive parts (anthers and stigma) ((Madjidian et al., 2008; Stout, 2000). For example, smaller
Osmia rufa (red mason bee) individuals are half as effective at pollinating canola as larger individuals probably due to intraspecific variation in the amount and position of pollen on their bodies and flower handling time (Jauker et al., 2016).
When a flower is visited by multiple pollinators during its receptive period (which is often the case to provide sufficient pollen to the stigma), the quality, quantity and composition of the received pollen loads will determine pollination success. This is dependent on the foraging behavior, sequence of pollinators and identity of pollinator
114 taxa in relation to the particular floral species (Willcox et al., 2017). Many plant species flower synchronously and sympatrically and many pollinators are generalists (Waser et al., 1996), resulting in pollinator sharing (Mitchell et al., 2009). Thus the floral community surrounding a particular plant and the foraging behavior of the pollinator community affects the amount of conspecific pollen received by a plant (Werrell et al.,
2016). Pollinator sharing can benefit plant reproduction when it results in more total pollinators in a plant community. In general, there is a positive correlation between floral abundance, pollinator abundance, and diversity (Kennedy et al., 2013; Potts et al., 2003;
Werrell et al., 2016). But pollinator sharing can be detrimental if too much heterospecific pollen transfer occurs causing stigma clogging with foreign pollen and a loss of receptive stigmatic surface area (Waser, 1986). In contrast, a higher number of conspecific pollen loads on the stigma is more likely to cause fruit production and increase seed production and weight in flowering plants (Bertin, 1990; Winsor et al., 1987). The competitive or facilitative nature of pollinator sharing depends on this balance of heterospecific versus conspecific pollen transfer and is density dependent, with the potential to shift from facilitative to competitive with increasing densities of one floral species (Rathcke, 1983;
Seifan et al., 2014; Willcox et al., 2017). The facilitative effect of pollinator sharing on pollination can occur via numerous mechanisms including: increasing floral display size which decreases overall interplant distance ((Rathcke, 1983; S. Feldman, 2006) and increases the number of flowers (Thomson, 1981), increasing diversity of floral stands
(Ghazoul, 2006), providing earlier blooming species that attract and maintain pollinator populations for later blooming species (Ogilvie and Thomson, 2016; Waser and Real,
115 1979), and a magnet species effect where an attractive plant species improves pollination success of a less attractive neighbor (Braun and Lortie, 2019; Laverty, 1992; Thomson,
1978).
Floral constancy is a foraging behavior that can measure how much pollinator sharing is occurring between co-flowering plants. It is exhibited by pollinators who sequentially visit the same species or floral morph, ignoring other equally rewarding species (Waser, 1986). It is common in social bee species but is also seen in other bees, insects and vertebrates (Goulson and Cory, 1993; Goulson and Wright, 1998) where individuals of the same colony or species specialize on different flower types. This behavior is beneficial to plant reproductive success because it lessens the possibility of heterospecific pollen transfer and increases the likelihood of conspecific pollen transfer
(Gegear and Laverty, 2005; Leebens-Mack and Milligan, 1998; Waser, 1986). However, environmental conditions such as the availability of floral resources, floral traits and floral rewards can cause individuals within a species to change from specialist to generalists (Grüter et al., 2011; Grüter and Ratnieks, 2011; Requier et al., 2015) . Floral constancy was previously proposed to be a result of learning and memory constraints in insects and birds (Waser, 1986) but more recent work has shown bee’s capacity to learn and recall information about multiple food resources. It is more likely due to the energy expenditure in switching flower types which require different handling techniques, which may be greater than the cost of searching for the same flower type (Amaya-Marquez,
2009).
116 The addition of co-flowering, sympatric floral species on crop fields through establishment of wildflower strips or hedgerows offers the benefits of being relatively low cost and easy to maintain for farmers while supporting ecosystem services and biodiversity on the farm (Morandin and Kremen, 2013) These types of restorations are often suggested in the scientific and extension literature but there is a lack of research on their real impacts on biodiversity and ecosystem services (Kleijn et al., 2006; Winfree,
2010). Key components that render these on-farm enhancements able to support pollination services include the age of a floral stand (Morandin and Kremen, 2013), density of other floral resources in comparison to the crop (Seifan et al., 2014), proximity to the additional floral resources (Samnegård et al., 2011) and nesting opportunities.
These additional floral resources are able to support a more diverse community of pollinators than monoculture agricultural systems which acts as a buffer against changes in bee abundances from year to year and from honey bee losses (Winfree et al., 2007).
For example, Kremen et al., (2002) saw large fluctuations in the pollinator community of watermelon in California from 2000 to 2001, with certain species being the most important and abundant pollinators one year and relatively unimportant the next year.
Various crop systems have shown the ability for additional floral resources to increase pollination services and yield for the crop by supporting a more diverse and abundant pollinator community on farms (i.e. mango (Carvalheiro et al., 2012), highbush blueberry (Blaauw and Isaacs, 2014), tomato (Balzan et al., 2016), and strawberry (Castle et al., 2019; Feltham et al., 2015)). However, some evidence indicates that crops and feral plants can compete for limited pollinators, resulting in negative effects on crop
117 pollination services (Ellis and Delaplane, 2009). This is a legitimate concern for growers wary of wildflowers drawing pollinators away from their crop (unpublished data). For example, in fields with co-flowering watermelon and sunflower, the onset of sunflower bloom corresponded with a decrease in honey bee visitation on watermelon and in fruit set and fruit size (Ellis and Delaplane, 2009). However, this study does not report the effect of co-flowering species on visitation by wild pollinators but notes the four-fold greater visitation by sweat bees (Halictidae) in watermelon flowers in their region, and similar visitation rates of bumble bees ( Bombus spp.) and squash bees ( Peponapis pruinosa ) in comparison with honey bees. In an agroecosystem equipped to support a diverse wild bee community, additional floral species may simply provide necessary food resources for a healthy pollinator community with positive effects on crop pollination.
Previous research shows that honey bees are not efficient pollinators of watermelon compared to wild bees because they deposit smaller amounts of pollen per visit, begin foraging later in the morning, and collect mostly nectar (Campbell et al.,
2018; Kremen et al., 2002; Pisanty et al., 2016; Winfree et al., 2007). For example,
Bombus impatiens is much more efficient at pollinating watermelon because individuals begin foraging 15-40 minutes before honey bees (watermelon stigmas are most receptive early in the morning), visited double the amount of flowers per minute than honey bees, and deposited almost three times as much pollen on watermelon stigmas it on average
(Stanghellini et al., 2002). Thus efforts to support a diverse community of wild pollinators may be critical for watermelon pollination, fruit quality and yield.
118 The potential for additional floral resources to negatively impact a crop’s pollination services is partly dependent on the foraging behavior and identity of the pollinator community. Previous work (chapter 2) showed that the majority of watermelon pollinators also foraged on wildflowers and/or weedy flowers when present in watermelon fields, an unsurprising result because most of the pollinator species in my study are generalists. However, if these insects exhibit floral constancy, there would be limited potential for heterospecific pollen transfer to occur. In this study I examine two components of pollinator foraging behavior that have not been studied in native watermelon pollinators (except for B. impatiens in Stanghellini et al., 2002): 1) flower handling time and 2) floral constancy. By investigating these two factors of pollinator behavior, my objective is to elucidate the different pollinator species’ overall effectiveness in this system and clarify whether watermelon and wildflowers share individual pollinators.
MATERIALS AND METHODS
Watermelon visitors were observed in 7 watermelon fields at the USDA
Vegetable Laboratory (2) and Clemson Coastal Research and Education Center (5) in
Charleston, SC during the floral anthesis period of Citrullus lanatus from June 30-August
2, 2016 and July 25-Aug 1, 2018. All fields were small at approximately 0.2 hectares, consisted of multiple varieties of triploid and diploid watermelon (SP7, Sugar Baby,
Charleston Grey, Crimson Sweet), and had either wildflower plantings or weedy flowers along one or both sides of the field. Wildflower plantings consisted of a ~60m x 1m strip of four floral species ( Cosmos sulphureus, Coreopsis tinctoria, Gaillardia pulchella,
119 Zinnia elegans ) that flower before, during and after watermelon bloom. Weedy flowers along field edges consisted mostly Verbena hastata and Trifolium spp. which co-flower with watermelon. For both types of data collection below, a bee landing on the central part of the flower where the stigma is located was counted as a visit (occasionally bees will land on flower petals to groom themselves or exhibit other behaviors that are clearly not foraging).
Flower handling time
Two to three observers trained in field pollinator identification recorded visitor group ( Agapostemon spp., Apis mellifera, Augochlorini, Bombus spp., Halictus sp.,
Lasioglossum spp., Megachile spp., Melissodes bimaculata, Melissodes communis, and
Xylocopa spp.) and the duration of individual visits (flower handling time) from 0930-
1200 EDST with a stopwatch. Temperature ranged from 80 - 90 degrees F and cloud cover from 0 - 70%. After one visit was timed, the observer moved to another location at least one row away and ~5m in either direction and recorded the next bee I saw, regardless of species. Thus, some of the data points may be from the same individual and thus not completely independent although I tried to avoid this.
Floral constancy
Two to three observers trained in field pollinator identification recorded visitor group ( Apis mellifera, Augochlorini, Bombus fraternus , B.impatiens, B.pensylvanicus,
B.griseocollis, Bombus sp., Lasioglossum spp., Megachile spp., and Melissodes bimaculata ) from 0915-1100 EDST in temperature ranging from 77 - 85 degrees F and cloud cover from 0 - 90%. Each observer followed the first bee seen as long as possible
120 up to 10 minutes, recording the number of visits the bee made and whether it moved between different floral species. Once the bee was lost or after 10 minutes, the observer moved to another location at least one row away and ~5m in either direction and recorded the next bee seen, regardless of species. Thus, some of the data points may be from the same individual and thus not completely independent although I tried to avoid this.
Statistical analysis
A one-way analysis of variance was used to test the effect of bee group on flower handling time, including date and date*species in the model. Post-hoc comparison using
Tukey’s HSD test was used to determine which bee groups differed in flower handling time. All significance tests used an alpha of 0.05. All statistical calculations were performed using JMP (Version 8, SAS Institute Inc, Cary, NC, USA).
RESULTS
Flower handling time
I observed 612 individual bee visits (396 in 2016 and 216 in 2018) on watermelon flowers in 7 watermelon fields. Mean flower handling time differed significantly between bee groups (F(9,602)=36.8, p<.0001) ranging from 2.7 seconds to 37.2 seconds per flower, with larger bees spending less time per flower (Table 3.1, Figure 3.1). Bumble bees ( Bombus spp.) and Eastern carpenter bees ( Xylocopa virginica ) had the fastest flower handling times (2.7 seconds SE ± 0.1, 2.7 SE ± 0.2, respectively), and the tiny sweat bees Lasioglossum spp. had the slowest flower handling time (37.2 SE ± 7.2), about 13 times slower than the fastest visitor. Post hoc comparisons using the Tukey
HSD test showed that Lasioglossum spp. mean flower handling time was significantly
121 lower than all the other bee species groups (p<0.0001). Also, mean flower handling time for Augochlorini (16.5 SE ± 2.9) was significantly lower than all the other bee groups
(p<.0001) except for Halictus spp. (9.3 SE ± 2.8). There was no evidence of nectar robbing behavior in any pollinators in this study. There was no significant effect of date or date*species in the ANOVA.
Floral constancy
I observed foraging behavior of 169 bees in 7 watermelon fields in 2016 and
2018. Of those 169 individuals, I observed 105 that started on watermelon flowers and 64 that started on another floral species in the watermelon field. There were 1487 floral visits (the combined number of flowers in foraging sequences) from bees that started on watermelon flowers and 600 floral visits from bees that started on another floral species.
I found that 16% of the bees that started on watermelon moved to another floral species at least once in their observed foraging sequence (Table 3.2). When all Bombus species were combined, 42% of individuals that began on watermelon switched floral species during their foraging bouts, much higher than the number of individuals of
Megachile spp., Lasioglossum spp. and Melissodes bimaculata that exhibited floral inconstancy (6%, 12.5%, and 12.5%, respectively).
Of the bees I observed starting on a different floral species in the watermelon field, 33% of them moved to a different floral species at least once in their observed foraging sequence (Table 3.2). Only Bombus spp. and Megachile spp. were observed starting on a different floral species and both genera had similar proportions of instances
122 where they switched floral species in a foraging sequence; 40% and 32% (for all Bombus species combined), respectively.
The length of foraging bouts observed differed substantially between bee species due to the small size, rapid and erratic flight and foraging behavior of certain bee species.
Thus, the mean number of flowers followed for Bombus spp. was 49 flowers in a sequence compared to mean of only 4 flowers for Lasioglossum spp. and 7 flowers for
Megachile spp.
DISCUSSION
I observed a significant difference in watermelon flower handling time amongst the bee pollinators, with larger bees spending less time per flower. In addition, most bees exhibited floral constancy both on watermelon and nearby wildflowers, however some individuals moved between floral species in their foraging bouts. While other studies have reported on the efficiency of native pollinators in terms of per-visit pollen deposition (Campbell et al., 2018; Kremen et al., 2002; Winfree et al., 2007), this study is the first to investigate the flower handling times (other than Bombus impatiens ) and floral fidelity of native pollinators of watermelon in the presence of co-flowering species.
Differences in flower handling time was likely due to variation in nectar extraction rates, tongue length, flower manipulation ability, age and naiveté of individuals, and relative size of the plant’s reproductive parts in relation to the pollinator’s body size (Ivey et al., 2003; Mitchell and Waser, 1992). In swamp milkweed
(Asclepias incarnata ), mean flower handling time was strongly correlated with pollen removal, pollen deposition, and pollination efficiency (Ivey et al., 2003), meaning that
123 increased pollination success should result from slower foraging time. A positive relationship between mean flower handling time and pollination success has been shown in several other flowering plant species as well (i.e. (Conner et al., 1995; Hurlbert et al.,
1996). In contrast, other studies show that pollinators that spent less time per flower had higher per visit pollen deposition rates and seed yield (Gomez and Zamora, 1999).
The relative importance of flower handling time is one element of the complex process of pollination. For example, in the case of the endemic herb Alstroemeria aurea, a native bumble bee ( Bombus dahlbomii ) spent more time per flower and was a significantly more efficient pollinator than its alien competitor ( Bombus ruderatus) , but the overwhelming abundance of the alien pollinator rendered it a more important contributor to the plant’s pollination success (Madjidian et al., 2008). This result agrees with other findings that visitation frequency is the most important predictor of a pollinator’s contribution to the plant’s reproductive success. This is because highly frequent pollinators usually contribute disproportionately to the plant’s pollination success even if their per-visit effectiveness is relatively low (Morris, 2015; Sahli and
Conner, 2006; Vázquez et al., 2005). Visitation frequency is in part a result of species abundance, meaning that rare species tend to have lower visitation frequency (Dupont et al., 2003; Vazquez and Aizen, 2006). The most effective pollinators are both abundant in an area and forage quickly from flower to flower (visitation rate component), coming into frequent contact with the stigma and transferring many pollen grains (pollen transfer component) (Rader et al., 2009).
124 Previous work (chapter 1) showed that out of the 6 pollinator groups I encountered, the smallest native bees (mostly Lasioglossum spp.) were the most frequent visitors of watermelon flowers in many of the watermelon fields, especially the fields with wildflowers. From 2016-2018, the average proportion of visits to watermelon flowers from this group alone ranged from 24 - 34% of all visits. Large bees ( Bombus spp. and Xylocopa spp.) and medium bees ( Melissodes spp., Halictus spp., and Megachile spp.) also contributed a large proportion of visits to watermelon flowers, with a combined mean contribution of 28 - 47%. Honey bees ranged from 20 - 29% of all visits on average from 2016-2018. Campbell et al., (2018) showed that Bombus impatiens and Melissodes spp. were the most effective at depositing pollen on watermelon flowers out of 5 bee genera on Florida watermelon fields. Agapostemon splendens deposited on average about half the amount of pollen per visit as B. impatiens, and Lasioglossum spp. deposited on average about a third the pollen deposition rate of B. impatiens (Campbell et al., 2018).
Similarly, Bombus californicus was efficient at depositing pollen on watermelon stigmas after just one visit but was not abundant on watermelon farms in California, while
Halictus tripartitus was a much more frequent visitor but did not deposit as much pollen per visit. When combined, these two species alone were able to provide ample pollination services to the watermelon crop in one year (Kremen et al., 2002). By combining visitation frequency on watermelon farms in the Northeast with pollen deposition rates,
Winfree et al., (2007) found that bumble bees alone pollinated the crop fully at 70% of farms and small bees (mostly Lasioglossum spp.) alone at 57% of farms, despite their low pollination efficiency on a per-flower basis. Many bee species were shared between my
125 study and Campbell et al., (2018) and Winfree et al. (2007), including B. impatiens, M. bimaculata, L. pilosum and L.imitatum, however there are differences in community composition. Nonetheless, in my study the relative inefficiency in per-visit pollen deposition of small bees ( Lasioglossum spp.) and their slow flower handling time may be outweighed by their frequency of visitation and floral constancy. Given the high efficiency per flower that Bombus spp. and Melissodes spp. display in previous studies, combined with their fast flower handling time and abundance in my fields, these two groups are arguably the most important pollinator groups for watermelon in this study region. However, I observed higher rates of floral inconstancy in Bombus spp. than in other groups which may negatively affect their pollination efficiency.
A diverse pollinator community creates a more stable and resilient pollination environment for pollinator-dependent crops than managed species alone because it includes a variety of foraging behaviors, per-flower efficiencies, body sizes, emergence periods, and temporal and spatial activities (Brittain et al., 2013; Pisanty et al., 2016). In apple orchards, pollination services were greater where there was a mix of bees with different, complementary qualities compared to orchards with honey bees alone. This was due to a combination of honey bees which are abundant but less effective, mining bees
(Andrena ) which are effective and abundant but slow foragers, and bumble bees which are less abundant but faster and able to forage in less favorable weather conditions
(Martins et al., 2015). The variety in flower handling time, floral constancy, per visit efficiency and temporal activity in the pollinator community of my study may reflect similar effects on watermelon pollination.
126 Previous work showed that most of the watermelon pollinator species in my study also foraged on one or more of the wildflower or weedy species in watermelon fields
(chapter 2). Despite the presence of multiple other rewarding floral species, most individuals exhibited floral constancy, a desirable trait for effective pollination because it reduces the possibility of heterospecific pollen transfer (Waser, 1986). Thus, individuals of the same species or colony (in social species) exhibited variation in floral choice but tend to be specialists on those species. In addition, watermelon flowers in fields with wildflowers received about the same number of visits as control fields without additional floral resources, but small native bees ( Lasioglossum spp.) were much more abundant when wildflowers were present (chapter 1). Thus, the wildflowers are likely not competing for pollination services but simply adding to the diversity of food resources, attracting and maintaining a diverse pollinator community
However, my results on floral constancy are biased toward larger bees because they were the easiest to follow for longer foraging sequences, so including more species may present new results. There was a lack of consistency in the number of flower visits I was able to follow per bee and a low sample size which impacts the certainty of floral constancy when the number of visits was very low. Lasioglossum spp. were sometimes very difficult to see on watermelon flowers because they forage so far into the flower with their head often under the stigma, so that much of their body is obscured by the stigma, and when they transition to another flower they move so erratically that they are easily lost. Megachile spp. and syrphid flies move quickly between flowers, sometimes only alighting a second or two before flying quickly to another location far away, thus
127 making them difficult to follow. Green bees ( Agapostemon spp. and Augochlorini) spend a few seconds on a flower, but also do not follow a sequence of flowers in close proximity and are easily lost after a single visit. Bombus spp., Xylocopa spp. and
Melissodes spp. move quickly from flower to flower but spend a few seconds longer per flower and often will move along a row so that they are easier to follow in a sequence.
Honey bees spend more time per flower and are easily followed as they fly or hover relatively slowly between flowers close to each other. Further research into floral constancy that includes measuring heterospecific pollen transfer on watermelon stigmas is necessary to account for these difficulties in following certain pollinators.
Flowers with different morphologies require different handling techniques which make switching between species more energetically costly than staying constant to one species (Heinrich, 1976). However, even species like honey bees known for their floral constancy can exhibit inconstancy in response to the amount of floral rewards available
(Grüter et al., 2011). Also, floral species with similar morphologies may require the same handling techniques, allowing the pollinator to switch between species without an energetic cost (Amaya-Marquez, 2009). Therefore, the differences in flower size, morphology, and rewards on my fields may have been great enough to promote floral constancy of pollinators and may be a key component to recommending floral mixes for farms. There also may be a density threshold at which wildflowers in an agricultural field compete with the crop for pollination services instead of facilitating or having a neutral effect (Rathcke, 1983). Choosing co-flowering species that flower before and after crop bloom but less during crop bloom would attract pollinators to the area and provide
128 enough food sources to maintain healthy populations while alleviating the potential for competition with the crop. Overall, the floral constancy I observed supports recommendations and growing evidence for providing floral resources in agricultural areas to support and attract a diverse native pollinator community. A diverse pollinator community, like the one observed in many of my watermelon fields, provides a more resilient and more stable pollination environment for watermelon and other pollinator- dependent crops than managed pollinators alone could provide (Brittain et al., 2013). The benefits of resilience and stabilization to the crop pollination services as well as the inherent value of biodiversity arguably outweigh the possibility that bees could move between floral species.
More research into the foraging behavior on flowers needs to be conducted to fully understand the effectiveness of native pollinators in watermelon pollination and other pollinator-dependent crops. No studies to date have investigated aspects of behavior specific to watermelon pollination like stigma contact, grooming behavior, whether pollinators are collecting pollen or nectar, and other in-flight and on-flower behaviors that can dictate pollinator effectiveness. This is the first study that records flower handling time for native bees other than B. impatiens on watermelon and to record the possibility of heterospecific pollen transfer between watermelon and co-flowering species in agricultural settings. A more complete assessment of this behavior should include examining heterospecific pollen loads per pollinator species on watermelon stigmas in addition to floral constancy behavior.
CONCLUSION
129 On farm enhancements with additional floral resources can support a more diverse community of wild pollinators so that pollination services are more resilient and robust to environmental change (Feltham et al., 2015; Kennedy et al., 2013; Morandin and Kremen, 2013). This study verifies previous results (chapter 1 and 2) suggesting that implementing wildflower strips and maintaining weedy flower edges on watermelon is beneficial to watermelon pollination services and the native pollinator community. I observed a range of foraging behaviors which may together complement each other to provide more effective pollination services. While Lasioglossum spp. had longer flower handling times and lower pollen deposition rates (Campbell et al., 2018; Kremen et al.,
2002; Winfree et al., 2007), its higher visitation frequency than most other pollinator groups across three years may outweigh its weaknesses in foraging efficiency.
Meanwhile, Bombus spp. had a much faster flower handling time on average, and a relatively high frequency of visitation, but showed some floral inconstancy on watermelon flowers. Other studies investigating pollinator effectiveness and native pollinator communities in crop systems should include foraging behaviors of each species to fully understand the likelihood of conspecific pollen transfer occurring.
REFERENCES
Amaya-Marquez, M., 2009. Floral constancy in bees: a revision of theories and a
comparison with other pollinators. Rev. Colomb. Entomol. 35, 206–216.
Andersson, G., Ekroos, J., Stjernman, M., Rundlof, M., Smith, H., 2014. Effects of
farming intensity, crop rotation and landscape heterogeneity on field bean
130 pollination. Agric. Ecosyst. Environ. 184, 145–148.
Balzan, M. V., Bocci, G., Moonen, A.-C., 2016. Utilisation of plant functional diversity
in wildflower strips for the delivery of multiple agroecosystem services. Entomol.
Exp. Appl. 158, 304–319. https://doi.org/10.1111/eea.12403
Bertin, R.I., 1990. EFFECTS OF POLLINATION INTENSITY IN CAMPSIS
RADICANS. Am. J. Bot. 77, 178–187. https://doi.org/10.1002/j.1537-
2197.1990.tb13544.x
Blaauw, B.R., Isaacs, R., 2014. Flower plantings increase wild bee abundance and the
pollination services provided to a pollination-dependent crop. J. Appl. Ecol. 51,
890–898. https://doi.org/10.1111/1365-2664.12257
Bosch, J., Blas, M., 1994. Foraging behaviour and pollinating efficiency of Osmia
cornuta and Apis mellifera on almond (Hymenoptera, Megachilidae and Apidae).
Appl. Entomol. Zool. 29, 1–9.
Braun, J., Lortie, C.J., 2019. Finding the bees knees: A conceptual framework and
systematic review of the mechanisms of pollinator-mediated facilitation. Perspect.
Plant Ecol. Evol. Syst. 36, 33–40. https://doi.org/10.1016/j.ppees.2018.12.003
Brittain, C., Kremen, C., Klein, A.-M., 2013. Biodiversity buffers pollination from
changes in environmental conditions. Glob. Chang. Biol. 19, 540–547.
https://doi.org/10.1111/gcb.12043
Brown, B.J., Mitchell, R.J., 2001. Competition for pollination: effects of pollen of an
invasive plant on seed set of a native congener. Oecologia 129, 43–49.
https://doi.org/10.1007/s004420100700
131 Campbell, J.W., Daniels, J.C., Ellis, J.D., 2018. Fruit Set and Single Visit Stigma Pollen
Deposition by Managed Bumble Bees and Wild Bees in Citrullus lanatus
(Cucurbitales: Cucurbitaceae). J. Econ. Entomol. 111, 989–992.
https://doi.org/10.1093/jee/toy008
Carvalheiro, L.G., Seymour, C.L., Nicolson, S.W., Veldtman, R., 2012. Creating patches
of native flowers facilitates crop pollination in large agricultural fields: mango as a
case study. J. Appl. Ecol. 49, 1373–1383. https://doi.org/10.1111/j.1365-
2664.2012.02217.x
Carvalheiro, L.G., Veldtman, R., Shenkute, A.G., Tesfay, G.B., Pirk, C.W.W.,
Donaldson, J.S., Nicolson, S.W., 2011. Natural and within-farmland biodiversity
enhances crop productivity. Ecol. Lett. 14, 251–259. https://doi.org/10.1111/j.1461-
0248.2010.01579.x
Castle, D., Grass, I., Westphal, C., 2019. Fruit quantity and quality of strawberries benefit
from enhanced pollinator abundance at hedgerows in agricultural landscapes. Agric.
Ecosyst. Environ. 275, 14–22. https://doi.org/10.1016/J.AGEE.2019.01.003
Conner, J.K., Davis, R., Rush, S., 1995. The effect of wild radish floral morphology on
pollination efficiency by four taxa of pollinators. Oecologia 104, 234–245.
https://doi.org/10.1007/BF00328588
Dupont, Y.L., Hansen, D.M., Olesen, J.M., 2003. Structure of a plant-flower-visitor
network in the high-altitude sub-alpine desert of Tenerife, Canary Islands.
Ecography (Cop.). 26, 301–310. https://doi.org/10.1034/j.1600-0587.2003.03443.x
Ellis, A., Delaplane, K.S., 2009. An evaluation of Fruit-Boost TM as an aid for honey bee
132 pollination under conditions of competing bloom. J. Apic. Res. 48, 15–18.
https://doi.org/10.3896/IBRA.1.48.1.04
Feltham, H., Park, K., Minderman, J., Goulson, D., 2015. Experimental evidence that
wildflower strips increase pollinator visits to crops. Ecol. Evol. 5, 3523–3530.
https://doi.org/10.1002/ece3.1444
Flanagan, R.J., Mitchell, R.J., Knutowski, D., Karron, J.D., 2009. Interspecific pollinator
movements reduce pollen deposition and seed production in Mimulus ringens
(Phrymaceae). Am. J. Bot. 96, 809–815. https://doi.org/10.3732/ajb.0800317
Gegear, R.J., Laverty, T.M., 2005. Flower constancy in bumble bees: a test of the trait
variability hypothesis. Anim. Behav. 69, 939–949.
Ghazoul, J., 2006. Floral diversity and the facilitation of pollination. J. Ecol. 94, 295–
304. https://doi.org/10.1111/j.1365-2745.2006.01098.x
Gomez, J., Zamora, R., 1999. Generalization vs. specialization in the pollination system
of Hormathophylla spinosa (Cruciferae). Ecology 80, 796–805.
https://doi.org/10.1890/0012-9658(1999)080[0796:GVSITP]2.0.CO;2
Goulson, D., Cory, J.S., 1993. Flower constancy and learning in foraging preferences of
the green-veined white butterfly Pleris napi. Ecol. Entomol. 18, 315–320.
https://doi.org/10.1111/j.1365-2311.1993.tb01107.x
Goulson, D., Wright NP, 1998. Flower constancy in the hoverflies Episyrphus balteatus
(Degeer) and Syrphus ribesii (L.) (Syrphidae). Behav. Ecol. 9, 213–219.
Grüter, C., Moore, H., Firmin, N., Helanterä, H., Ratnieks, F.L.W., 2011. Flower
constancy in honey bee workers (Apis mellifera) depends on ecologically realistic
133 rewards. J. Exp. Biol. 214, 1397–402. https://doi.org/10.1242/jeb.050583
Grüter, C., Ratnieks, F.L.W., 2011. Flower constancy in insect pollinators: Adaptive
foraging behaviour or cognitive limitation? Commun. Integr. Biol. 4, 633–636.
https://doi.org/10.4161/cib.16972
Heinrich, B., 1976. Bumblebee Foraging and the Economics of Sociality. Am. Sci. 64,
384–395.
Herrera, C., 1987. Components of Pollinator “Quality”: Comparative Analysis of a
Diverse Insect Assemblage. Oikos 50, 79–90.
Hurlbert, A.H., Hosoi, S.A., Temeles, E.J., Ewald, P.W., 1996. Mobility of Impatiens
capensis flowers: effect on pollen deposition and hummingbird foraging. Oecologia
105, 243–246. https://doi.org/10.1007/BF00328553
Ivey, C.T., Martinez, P., Wyatt, R., 2003. Variation in pollinator effectiveness in swamp
milkweed, Asclepias incarnata (Apocynaceae). Am. J. Bot. 90, 214–225.
https://doi.org/10.3732/ajb.90.2.214
Jauker, F., Speckmann, M., Wolters, V., 2016. Intra-specific body size determines
pollination effectiveness. Basic Appl. Ecol. 17, 714–719.
https://doi.org/10.1016/j.baae.2016.07.004
Karron, J.D., Mitchell, R.J., Bell, J.M., 2006. Multiple pollinator visits to Mimulus
ringens (Phrymaceae) flowers increase mate number and seed set within fruits. Am.
J. Bot. 93, 1306–1312. https://doi.org/10.3732/ajb.93.9.1306
Kennedy, C.M., Lonsdorf, E., Neel, M.C., Williams, N.M., Ricketts, T.H., Winfree, R.,
Bommarco, R., Brittain, C., Burley, A.L., Cariveau, D., Carvalheiro, L.G., Chacoff,
134 N.P., Cunningham, S.A., Danforth, B.N., Dudenhöffer, J.-H., Elle, E., Gaines, H.R.,
Garibaldi, L.A., Gratton, C., Holzschuh, A., Isaacs, R., Javorek, S.K., Jha, S., Klein,
A.M., Krewenka, K., Mandelik, Y., Mayfield, M.M., Morandin, L., Neame, L.A.,
Otieno, M., Park, M., Potts, S.G., Rundlöf, M., Saez, A., Steffan-Dewenter, I., Taki,
H., Viana, B.F., Westphal, C., Wilson, J.K., Greenleaf, S.S., Kremen, C., 2013. A
global quantitative synthesis of local and landscape effects on wild bee pollinators in
agroecosystems. Ecol. Lett. 16, 584–599. https://doi.org/10.1111/ele.12082
Kleijn, D., Baquero, R.A., Clough, Y., Díaz, M., Esteban, J., Fernández, F., Gabriel, D.,
Herzog, F., Holzschuh, A., Jöhl, R., Knop, E., Kruess, A., Marshall, E.J.P., Steffan-
Dewenter, I., Tscharntke, T., Verhulst, J., West, T.M., Yela, J.L., 2006. Mixed
biodiversity benefits of agri-environment schemes in five European countries. Ecol.
Lett. 9, 243–254. https://doi.org/10.1111/j.1461-0248.2005.00869.x
Kremen, C., Williams, N.M., Thorp, R.W., 2002. Crop pollination from native bees at
risk from agricultural intensification. Proc. Natl. Acad. Sci. U. S. A. 99, 16812–6.
https://doi.org/10.1073/pnas.262413599
Laverty, T.M., 1992. Plant interactions for pollinator visits: a test of the magnet species
effect. Oecologia 89, 502–508. https://doi.org/10.1007/BF00317156
Leebens-Mack, J., Milligan, B.G., 1998. Pollination biology in hybridizing Baptisia
(Fabaceae) populations. Am. J. Bot. 85, 500–507. https://doi.org/10.2307/2446433
Madjidian, J.A., Morales, C.L., Smith, H.G., 2008. Displacement of a native by an alien
bumblebee: Lower pollinator efficiency overcome by overwhelmingly higher
visitation frequency. Oecologia 156, 835–845. https://doi.org/10.1007/s00442-008-
135 1039-5
Martins, K.T., Gonzalez, A., Lechowicz, M.J., 2015. Pollination services are mediated by
bee functional diversity and landscape context. Agric. Ecosyst. Environ. 200, 12–20.
https://doi.org/10.1016/j.agee.2014.10.018
Mitchell, R., Flanagan, R., Brown, B., Waser NM, Karron JD, 2009. New frontiers in
competition for pollination. Ann. Bot. 103, 1403–1413.
Mitchell, R.J., Waser, N.M., 1992. Adaptive Significance of Ipomopsis Aggregata Nectar
Production: Pollination Success of Single Flowers. Ecology 73, 633–638.
https://doi.org/10.2307/1940769
Morandin, L.A., Kremen, C., 2013. Hedgerow restoration promotes pollinator
populations and exports native bees to adjacent fields. Ecol. Appl. 23, 829–839.
https://doi.org/10.1890/12-1051.1
Morris, W.F., 2015. Which Mutualists are Essential? Buffering Plant Reproduction, in:
The Importance of Species : Perspectives on Expendability and Triage. Princeton
University Press, pp. 260–280.
Ne’eman, G., Jürgens, A., Newstrom-Lloyd, L., Potts, S.G., Dafni, A., 2010. A
framework for comparing pollinator performance: effectiveness and efficiency. Biol.
Rev. 85, no-no. https://doi.org/10.1111/j.1469-185X.2009.00108.x
Ogilvie, J.E., Thomson, J.D., 2016. Site fidelity by bees drives pollination facilitation in
sequentially blooming plant species. Ecology 97, 1442–1451.
https://doi.org/10.1890/15-0903.1
Pisanty, G., Afik, O., Wajnberg, E., Mandelik, Y., 2016. Watermelon pollinators exhibit
136 complementarity in both visitation rate and single-visit pollination efficiency. J.
Appl. Ecol. 53, 360–370. https://doi.org/10.1111/1365-2664.12574
Potts, S.G., Vulliamy, B., Dafni, A., Ne’eman, G., Willmer, P., 2003. LINKING BEES
AND FLOWERS: HOW DO FLORAL COMMUNITIES STRUCTURE
POLLINATOR COMMUNITIES? Ecology 84, 2628–2642.
https://doi.org/10.1890/02-0136
Rader, R., Howlett, B.G., Cunningham, S.A., Westcott, D.A., Newstrom-Lloyd, L.E.,
Walker, M.K., Teulon, D.A.J., Edwards, W., 2009. Alternative pollinator taxa are
equally efficient but not as effective as the honey bee in a mass flowering crop. J.
Appl. Ecol. 46, 1080–1087. https://doi.org/10.1111/j.1365-2664.2009.01700.x
Rathcke, B., 1983. Competition and Facilitation Among Plants for Pollination, in: Real,
L. (Ed.), Pollination Biology. Elsevier, p. 305-.
Requier, F., Odoux, J.-F., Tamic, T., Moreau, N., Henry, M., Decourtye, A., Bretagnolle,
V., 2015. Honey bee diet in intensive farmland habitats reveals an unexpectedly
high flower richness and a major role of weeds. Ecol. Appl. 25, 881–890.
https://doi.org/10.1890/14-1011.1
S. Feldman, T., 2006. Pollinator aggregative and functional responses to flower density:
does pollinator response to patches of plants accelerate at low-densities? Oikos 115,
128–140. https://doi.org/10.1111/j.2006.0030-1299.14493.x
Sahli, H.F., Conner, J.K., 2006. Characterizing ecological generalization in plant-
pollination systems. Oecologia 148, 365–372. https://doi.org/10.1007/s00442-006-
0396-1
137 Samnegård, U., Persson, A.S., .Smith, H.G., 2011. Gardens benefit bees and enhance
pollination in intensively managed farmland. Biol. Conserv. 144, 2602–2606.
Seifan, M., Hoch, E.-M., Hanoteaux, S., Tielbörger, K., 2014. The outcome of shared
pollination services is affected by the density and spatial pattern of an attractive
neighbour. J. Ecol. 102, 953–962. https://doi.org/10.1111/1365-2745.12256
Stanghellini, M.S., Ambrose, J.T., Schultheis, J.R., 2002. Diurnal activity, floral
visitation and pollen deposition by honey bees and bumble bees on field-grown
cucumber and watermelon. J. Apic. Res. 41, 27–34.
https://doi.org/10.1080/00218839.2002.11101065
Stout, J., 2000. Does size matter? Bumblebee behaviour and the pollination of Cytisus
scoparius L.(Fabaceae). Apidologie 31, 129–139.
Thomson, J., 1981. Spatial and temporal components of resource assessment by flower-
feeding insects. J. Anim. Ecol. 50, 49–59.
Thomson, J., 1978. Effects of stand composition on insect visitation in two-species
mixtures of Hieracium. Am. Midl. Nat. 100, 431–440.
Vazquez, D.P., Aizen, M.A., 2006. Community-wide Patterns of Specialization in Plant-
Pollinator Interactions Revealed by Null Models, in: Waser, N.M., Ollerton, J.
(Eds.), Plant-Pollinator Interactions: From Specialization to Generalization.
University of Chicago Press, pp. 200–216.
Vázquez, D.P., Morris, W.F., Jordano, P., 2005. Interaction frequency as a surrogate for
the total effect of animal mutualists on plants. Ecol. Lett. 8, 1088–1094.
https://doi.org/10.1111/j.1461-0248.2005.00810.x
138 Wallace, H.M., Maynard, G. V, Trueman, S.J., 2002. Insect flower visitors, foraging
behaviour and their effectiveness as pollinators of Persoonia virgata R. Br.
(Proteaceae). Aust. J. Entomol. 41, 55–59. https://doi.org/10.1046/j.1440-
6055.2002.00265.x
Waser, N., Real, L., 1979. Effective mutualism between sequentially flowering plant
species. Nature.
Waser, N.M., 1986. Flower Constancy: Definition, Cause, and Measurement. Am. Soc.
Nat. 127, 593–603.
Waser, N.M., Chittka, L., Price, M. V., Williams, N.M., Ollerton, J., 1996.
Generalization in Pollination Systems, and Why it Matters. Ecology 77, 1043–1060.
https://doi.org/10.2307/2265575
Werrell, P.A., Langellotto, G.A., Morath, S.U., Matteson, K.C., 2016. The Influence of
Garden Size and Floral Cover on Pollen Deposition in Urban Community Gardens.
Cities Environ. 2, 1–16. https://doi.org/10.15365/cate.2162009
Willcox, B.K., Aizen, M.A., Cunningham, S.A., Mayfield, M.M., Rader, R., 2017.
Deconstructing pollinator community effectiveness. Curr. Opin. Insect Sci. 21, 98–
104. https://doi.org/10.1016/j.cois.2017.05.012
Winfree, R., 2010. The conservation and restoration of wild bees. Ann. N. Y. Acad. Sci.
1195, 169–197. https://doi.org/10.1111/j.1749-6632.2010.05449.x
Winfree, R., Williams, N.M., Dushoff, J., Kremen, C., 2007. Native bees provide
insurance against ongoing honey bee losses. Ecol. Lett. 10, 1105–1113.
https://doi.org/10.1111/j.1461-0248.2007.01110.x
139 Winsor, J.A., Davis, L.E., Stephenson, A.G., 1987. The Relationship between Pollen
Load and Fruit Maturation and the Effect of Pollen Load on Offspring Vigor in
Cucurbita pepo. Am. Nat. 129, 643–656. https://doi.org/10.1086/284664
Woodcock, B.A., Edwards, M., Redhead, J., Meek, W.R., Nuttall, P., Falk, S.,
Nowakowski, M., Pywell, R.F., 2013. Crop flower visitation by honey bees, bumble
bees and solitary bees: Behavioural differences and diversity responses to landscape.
Agric. Ecosyst. Environ. 171, 1–8. https://doi.org/10.1016/j.agee.2013.03.005
Young, H.J., Stanton, M.L., 1990. Influences of Floral Variation on Pollen Removal and
Seed Production in Wild Radish. Ecology 71, 536–547.
https://doi.org/10.2307/1940307
140 Species n Mean Duration of Visit (seconds) SE (seconds) Bombus spp. 137 2.7 0.1 Xylocopa virginica 39 2.7 0.2 Melissodes communis 72 3.5 0.3 Melissodes bimaculata 121 3.6 0.3 Agapostemon sp. 31 4.1 0.5 Megachile spp. 53 4.4 0.5 Apis mellifera 69 5.7 0.5 Halictus sp. 11 9.3 2.8 Augochlorini 50 16.5 2.9 Lasioglossum spp. 29 37.2 7.2
Table 3.1 Duration of visits per pollinator species on single watermelon flowers in South Carolina watermelon fields
141 Figure 3.1 Flower handling time in seconds per bee species on C. lanatus flowers . Central lines are medians, boxes represent interquartile range and whiskers represent 10%/90% quantiles. Bee groups were identified in the field and not collected, but other research (chapter 2) involving collecting pollinators foraging on C. lanatus flowers in the same fields showed that the only Agapostemon species collected was A. splendens, Augochlorini collected were mostly Augochlorella aurata, but also Augochlora pura, Auglochloropsis metallica fulgida, and Augochloropsis sumptuosa, Bombus species consisted of B. impatiens, B. fraternus, B. griseocollis and B. pensylvanicus, Halictus species were mostly H. poeyi but also H. rubicundus, Lasioglossum species was mostly L. callidum but also 16 other species, Megachile species were mostly M. mendica but also M. petulans, M. pseudobrevis, M. texana, and M. xylocopoides .
142 A. Citrullus lanatus Bee group n Mean #flowers followed Switched species/Total Augochlorini 8 5 0/8 0% Bombus fraternus 2 67 1/2 50% B. griseocollis 4 43 3/4 75% B. impatiens 16 25 4/16 25% B. pensylvanicus* 2 62 2/2 100% Lasioglossum spp. 24 4 3/24 12.5% Melissodes bimaculata 16 19 2/16 12.5% Megachile spp. 33 7 2/33 6% Total 105 29 17/105 16% *All Bombus species combined: N=24, Mean flowers followed=49, Switched species/total=10/24 42%
B. Other species ( Cosmos sulphureus, Gaillardia pulchella, Rudbeckia hirta, Zinnia elegans, Trifolium sp.) Bee group n Mean #flowers followed Switched species/Total Bombus sp. 19 10 6/19 31.5% B. fraternus 8 26 3/8 38% B. griseocollis 4 40 2/4 50% B. impatiens 7 9 2/7 28.5% B. pensylvanicus** 21 22 6/21 28.5% Megachile spp. 5 8 2/5 40% Total 64 21 21/64 33% ** All Bombus species combined: N=59, Mean flowers followed=21, Switched species/total=19/59 32%
Table 3.2 Floral constancy exhibited by bee pollinators of Citrullus lanatus on watermelon fields with co-flowering wildflowers and watermelon. A. Bees observed that started on C. lanatus B. Bees observed that started on another floral species. “Mean flowers followed” is the mean number of flowers observed in a foraging sequence by one observer. “Switched species/total” is the number of individuals that moved between floral species in an observed foraging sequence.
143 CHAPTER 4 PLANTING WILDFLOWER STRIPS ON WATERMELON FIELDS TO SUPPORT NATIVE POLLINATOR BIODIVERSITY 1
My goal is to provide information relevant to watermelon growers and the conservation community in South Carolina and condense research that pertains to important topics for pollination in this crop system. I clarify why supporting native pollinators is critical to the future of food security, agriculture, and natural ecosystems. I address five questions: 1. Why conserve biodiversity of the pollinator community? 2. Why include on-farm enhancements? 3. How can I enhance native pollinators on farms? 4. Could wildflowers draw pollinators away from my crop or have other negative effects? 5. What are the most common native pollinators on watermelon fields in South Carolina and how can I protect them?
1. Why conserve biodiversity of the pollinator community?
Globally, pollinators are declining at alarming rates due to a combination of habitat loss and corresponding lack of food resources, increased pests, parasites, and pesticide use (Goulson et al., 2015). The Intergovernmental Science-Policy Platform on
Biodiversity and Ecosystem Services estimated that 40% of the world’s invertebrate pollinators are at risk of extinction (IPBES, 2016) but there is still little to no information about many wild species (Goulson et al., 2015). The European honey bee
Apis mellifera remains the most important managed agricultural tool for pollination but is facing multiple threats, including the introduction of Varroa mites and overexposure to pesticides, resulting in average annual colony losses in the US of 40-50% since 2006
(Lee et al., 2015). Our current reliance on a small number of managed species, mostly the honey bee, for pollination services, is unsustainable (Brittain et al., 2013). One
reason is that more than 75% of the world’s leading food crops rely on animal pollination for maximum quality and yield and reliance on a single species demonstrably vulnerable to disease is risky (Klein et al., 2006). In addition, many crops produce more fruit or better quality fruit when a more diverse community of pollinators contribute to pollinating the crop (Garibaldi et al., 2014). Wild bees improve seed set, quality, shelf-life and commercial value of many crops (Winfree et al., 2011) and are more efficient pollinators of certain crops including watermelon (Winfree et al., 2007).
Wild pollinators also pollinate about 2/3 of wild flowering plants in natural ecosystems, providing food in the form of plants, seeds and fruits for other wildlife from birds to bears. Therefore, protecting these keystone species is critical for the future of the food supply and functioning ecosystems alike.
Watermelon is the largest acreage vegetable crop grown in South Carolina. It has separate male and female flowers, making it completely dependent on pollinators to set fruit by moving pollen from the male flowers to the stigmas of the female flowers. Insufficient pollination can lead to misshapen fruit and poor yields.
Many in the agricultural industry and conservation community are unaware of the actual diversity and services provided by wild native pollinators. In my study in central and coastal South Carolina watermelon fields, I observed and collected 59 species of native pollinators that visited watermelon in 2016, 2017 and 2018. Most of these were bees in the families Halictidae, Apidae, and Megachilidae. Native pollinators
145 provided most of the flower visits (71-80% of visits) to watermelon on 21 fields, despite honey bee hive placement near all fields for pollination. Of those native bee visits, tiny sweat bees ( Lasioglossum spp.) made up 24-34% of visits depending on the year, large bees (bumble bees and carpenter bees) made up 14-29% of visits, medium bees (long- horned bees, leafcutter bees, medium-sized sweat bees) made up 10-22% of visits, green bees made up 2-4%, and other insects 4-7%. Previous research showed that wild bees, especially bumble bees and long-horned bees, are much more efficient pollinators of watermelon on a per-visit basis than honey bees by depositing more pollen each time they land on a female flower (Campbell et al., 2018). Many wild bees also forage earlier in the morning than honey bees when watermelon flowers are most receptive and in more adverse weather conditions (Stanghellini et al., 2002). Therefore, the wild pollinator community of watermelon in South Carolina provides critical pollination services for this crop. Watermelon growers should consider implementing on-farm efforts to conserve a diverse pollinator community for the future of this and other pollinator-dependent crops.
Average proportion of watermelon flower visits contributed by 6 pollinator groups over 3 years on 21 watermelon fields in South Carolina. Wild bees, made up of 4 groups and 50 species, contributed the majority of visits in all 3 years but the proportions of each group varied by year and by field.
146
Habitat loss. Native bees require habitat that provides them food (flowers) and shelter (nesting materials and appropriate habitat). Other non-bee pollinators share in common the need for floral resources but exhibit different natural histories and different area requirements from bees. For example, hover flies (Syrphidae) do not have nests and thus do not require nesting sites like bees; others require certain plant hosts or prey in their larval stage, such as Monarch butterflies and milkweed. Some fields provide all the resources wild pollinators need. For example, most fields in our study were small, allowed weedy flowers to grow in ditches and unused areas, included wildflower strips, and were part of a polyculture (multiple crop types) system. Thus, the environmental conditions of the fields and edges in our study likely provided enough habitat and food resources for a relatively diverse community of pollinators. More research would reveal how far these pollinators travel to access habitat.
If habitats are not available on fields as may be the case in larger more homogenous field systems, then wild pollinators would depend on areas farther away or may not be able to find refuging habitat, and fail to persist. High rates of land use change and urbanization in the Charleston area, in accordance with global trends for coastal cities (Neumann et al., 2015), would likely affect native pollinator communities and other wildlife on coastal farms. Charleston became the largest city in South Carolina in 2017 with a 12.4% population change from 2010-2017 (from ~120,000-135,000 residents). Mt. Pleasant, a suburb of Charleston, is the fastest growing suburban town in
South Carolina, nearly doubling in population from 2000-2017 (US Census Bureau).
Uncontrolled, unplanned growth consuming a disproportionate amount of land, or urban sprawl, has dominated urbanization trends in this region. From 1973 to 1994, a
147 one percent increase in population in the Charleston area resulted in a six percent loss in forest and farm land (Allen and Wu, 2002). Urbanization leads to a less diverse pollinator community with a bias towards more common, generalist species (Deguines et al., 2016). Specialist bees, butterflies and flies that rely on a small range or one type of pollen or larval host are most vulnerable to land-use change (Winfree et al., 2011).
Habitat loss and fragmentation, a consequence of urbanization, is most likely the key factor driving bee declines (Potts et al., 2010) and in general is negatively correlated with wild bee abundance and species richness (Ricketts et al., 2008). The amount of high quality habitat surrounding a farm in combination with local-scale field diversity and organic management are the most important factors that support wild bee communities. In simplified monoculture fields, the surrounding habitat becomes more important, and the benefits of on-farm diversification and management become greater
(Kennedy et al., 2013). On average, fields 1.5 km away from natural habitat patches can be expected to contain 50% of the pollinator diversity of fields closest to these patches
(Ricketts et al., 2008). Larger-bodied pollinators can forage longer distances from their nests (Greenleaf et al., 2007), so with increasing distance from natural habitat, fewer pollinator species are able to either forage to that distance or nest in fields so isolated from native resources (Ricketts et al., 2008). Social bees like bumble bees and some ground nesting bees are more negatively affected by land-use change than solitary bees, possibly due to pesticide bioaccumulation in the larger nests of social species (Williams et al., 2010). Species that nest above ground in pre-existing cavities (such as bumble bees and leafcutter bees) are more sensitive to disturbance and isolation from natural habitat than ground nesting bees or species that excavate their own nests (such as carpenter bees). This may result from above-ground nest sites becoming more limited
148 with increasing disturbance whereas bare soil may become more available (Williams et al., 2010). However, urbanization can provide a filter for the bee community, benefitting some bee species, cavity-nesters and exotic species especially, by creating more nesting opportunities in the form of wood sheds, fences, trees and homes but limiting opportunities for ground-nesting or above- ground nesting species (Matteson et al.,
2008).
In contrast, almost half of the 48 counties in South Carolina show trends of declining population mostly in rural areas (Tippett, 2015) so the same threats from urbanization may not apply to the pollinator populations there. Instead, agricultural intensification may result from declining human population in these regions. From local to landscape scale, agricultural intensification is generally correlated with a decrease in abundance, diversity and pollination services of native pollinators (Kremen and
Chaplin-Kramer, 2007). This detrimental effect on pollinators is due to a combination of the effects of increased pesticide use, destruction of nest sites from tillage and removal of woody vegetation, loss of natural to seminatural habitat and decreased crop and weed diversity (Kremen et al., 2007). Bee species that nest above ground are more negatively affected by agricultural intensification than species that nest below ground (Williams et al., 2010). However, agricultural areas, when not intensively managed, can provide habitat for pollinators especially when they break up landscapes dominated by forests
(Tscharntke et al., 2005).
149 A resilient and stable pollinator community includes a diverse suite of pollinators with a range of nesting habits, foraging behaviors, and activity periods. These different behaviors and life history traits complement each other and can buffer against year to year fluctuations or environmental changes that affect pollinator species differently.
Most watermelon fields in our study in South Carolina were on diversified farms, including multiple crop types, weedy flowers on field edges or wildflower strips and were part of a more heterogenous landscape, with forest edges lining fields and fallow fields nearby. These farm conditions are better able to support insects and other wildlife than intense monoculture agriculture, likely resulting in the diverse community of pollinators we observed. Pictured is Rosebank Farm on John’s Island, SC. 2. Why include on-farm enhancements? Native bees have two basic needs: flowers and nesting sites. Other pollinators may need nesting areas but may require certain plant hosts for their larvae, such as the
Monarch butterfly and milkweed. Protecting pollinators and the services they provide on farms can be achieved by improving on-farm management practices in addition to protecting high quality habitat around farms (Kennedy et al., 2013). One commonly suggested method of improving conditions for pollinators in agro-landscapes is planting alternative floral resources, i.e. wildflower strips or hedgerows, to increase floral
150 diversity, food resources and potential nesting resources. Wildflowers and hedgerows can provide food and nesting resources for bees and other pollinators, as well as predatory and parasitic insects, enhancing species richness and abundance of these beneficial insects (Garibaldi et al., 2014). Beyond providing resources and habitats for agrobiodiversity, specific techniques such as the use of hedgerows or wildflower strips may also enhance the connectivity of landscapes which can benefit other wildlife species
(Kremen and Merenlender, 2018).
Charleston study. From 2016-2018, I studied the effects of implementing wildflower strips on South Carolina watermelon fields in terms of the diversity of watermelon pollinators, the number of visits to watermelon flowers and the diversity of the whole pollinator community in comparison with control fields that did not have wildflower plantings. The wildflower strips consisted of four native plant species ( Zinnia elegans, Gaillardia pulchella, Coreopsis tinctoria, Cosmos sulphureus), chosen for their drought-tolerance, fast germination rates, hardiness, difference in flowering period, length of flowering period, and attractiveness to a variety of pollinating insects.
151 Wildflower seedling s were transplanted after a month of growth in seed trays on the edges of watermelon fields in April, before watermelon transplants were put in the fields (L). The flowering period of the wildflowers began in May before watermelon bloom and lasted into August, long after watermelon was done flowering. The total area was relatively small at 3’ wide and 200-300’ long. The wildflowers were irrigated to ensure abundant bloom and survival, but at one site they were not irrigated and took longer to develop but survived and flowered later. A lower maintenance method would be broadcasting wildflower seeds in the fall for spring germination.
My study showed that when wildflowers were on the field, the number of visits to watermelon was significantly higher for one group of pollinators, tiny sweat bees. These small, metallic grey-green bees nest underground, vary from solitary to social depending on the species, and do not forage more than a few hundred meters from their nest
(Gibbs, 2011). Despite their low efficiency in depositing pollen on watermelon flowers
(Campbell et al., 2018), their high visitation frequency, which is considered the most important factor in determining a pollinator’s overall efficiency (Vázquez et al., 2005), may render them important pollinators in this system. In one year, honey bee visitation was significantly higher in control fields than in fields with wildflowers. This may have been a result of limited resources available for wild pollinators in control fields.
152 Tiny sweat bees (Lasioglossum spp.) pictured here on Zinnia, are so small they often go unnoticed. They were the most frequent watermelon visitors on many fields in our study and were the most frequently collected bees as well. Sixteen species of these bees were collected visiting watermelon.
Overall, the biodiversity of the pollinator community was higher in watermelon fields with increased floral diversity, with nearly twice the number of pollinator species collected on watermelon fields with wildflowers compared to control fields. In addition, the species richness of pollinators collected visiting watermelon flowers was slightly higher in fields with higher floral diversity than those with only watermelon flowers. The mean number of watermelon pollinating species per field was approximately 15 species
(14.5 species, 15.8 species and 16.3 in 2018, 2017 and 2016 respectively). The mean number of total pollinators (including wildflower pollinators) per field was about 24 species (23 species, 27 species and 22 species in 2018, 2017 and 2016, respectively).
The Southern plains bumble bee (Bombus fraternus) (L) and American bumble bee ( Bombus pensylvanicus) (R) were frequent watermelon and wildflower pollinators on farms in SC. They are considered endangered and vulnerable by the IUCN, respectively, with large recent declines in populations and geographic range.
More than half (64%) of the watermelon pollinator species we collected were also collected on one or more of five wildflower species in our study, demonstrating that social colonies of bees, solitary bees, and other insects like syrphid flies and butterflies use the multiple floral species as resources on the watermelon field in addition to the
153 crop flowers when they are available. In fields with wildflowers, we also observed or collected a wide range of pollinators and insects that do not pollinate watermelon but used the other floral resources available. In total combining pollinators collected and observed on both wildflowers and watermelon, 82 insect species visited the six most common floral species on watermelon fields in our study. Therefore, when wildflowers and weedy flowers are available on the farm landscape, a more diverse community of beneficial insects is supported. This community included declining species like Monarch butterflies, the American bumble bee and the Southern plains bumble bee and parasitic and predatory flies and wasps that can control crop pests.
Incorporating wildflowers on watermelon fields supports insect biodiversity of non-crop pollinators as well as crop pollinators. In South Carolina watermelon fields, wildflowers attracted a variety of non-watermelon visitor insects like bee flies (Bombyliidae), Palamedes swallowtails ( Papilio palamedes) , Monarch butterflies ( Danaus plexippis) , and sunflower bees (Svastra spp.). Beyond pollinating crops and contributing to the human food system, wild pollinators have intrinsic value that cannot be monetized.
154 On Rosebank Farm on John’s Island, SC, farmer Sidi Limehouse incorporates wildflower meadows and strips on his farm as part of his crop rotation and in any unused areas of the farm. He harvests a portion of the flowers to sell as cut flowers and bouquets at his roadside farm stand along with watermelon and several other crops he grows.
3. How to enhance native pollinators on farms? Three main components of on-farm management should be considered to improve
abundance and richness of native pollinators, especially bees.
1. Increasing floral resources 2. Increasing nesting sites 3. Reducing pesticide use
Increasing floral resources. Increasing floral resources on farms can be achieved in multiple ways. Planting wildflower strips in or along the edges of fields, especially if using drought-tolerant perennials, is a low-maintenance way to provide food for pollinators beyond the crop bloom period. Wildflower seeds can be broadcast in the fall for spring germination. Introducing a variety of flower species that vary in their flowering period, preferably extending from early spring to late fall, will ensure that pollinators that emerge or are active at different times of the year have sufficient food resources. Planting native species is encouraged as they will attract a more diverse suite of pollinators than non-native plants. A list of native plants that are well suited for the southeastern US can be found at https://xerces.org/pollinator-conservation/plant-
155 lists/pollinator-plants-southeast-region/. Hedgerows are a similar method that usually incorporate woody vegetation like shrubs and trees and can provide other services for a crop field such as a wind break. Planting flowering cover crops to rotate fields, improve soil conditions or prevent erosion can also serve as an opportunity to provide a food source for some pollinators. Most cover crops are non-native plants so they are likely to only attract more common pollinator species that are able to adapt to a wide variety of floral types (Vaughan et al., 2015). For example, white clover ( Trifolium repens) planted in watermelon fields in our area most commonly attracted European honey bees and the
Common Eastern bumble bee. Therefore, flowering cover crops should be considered a supplemental floral resource in addition to high quality native plant habitat. Planting a wider variety of flowering crops would also provide a more diverse floral environment for pollinators, in addition to helping prevent pest outbreaks. Lastly, retaining non- invasive weedy flowers in ditches, field edges and other non-arable areas by reducing herbicide spraying and mowing can provide important food sources for pollinators and refugia for natural enemies of crop pests. Verbena ( Verbena hastata) , wild vetch ( Vicia sativa) and wild radish ( Raphanus raphanistrum) were some of the common weedy plant species close to watermelon fields in our study, and many pollinators also forage on these species.
156 Bumble bee queens, such as this Southern plains bumble bee (Bombus fraternus) queen, emerge in early spring and are the sole foundresses of their colonies, consisting of hundreds of workers. They require plenty of early spring to late fall flowers to ensure a healthy colony.
Indian blanket (Gaillardia pulchella) (L) and Plains coreopsis ( Coreopsis tinctoria) (R) are easy to grow, perennial, drought-tolerant native wildflowers to the southeast that attract a wide variety of pollinators and other insects
Increasing nesting sites. Nesting sites for bees on watermelon fields in South
Carolina should include consideration of the two main types of nesting habits exhibited by bees in our study: ground-nesting (61% of pollinating species) and cavity-nesting
(26% of pollinating species). Ground nesting bees tend to be the most common bees in agricultural areas, possibly due to the availability of nest sites compared to the needs of cavity-nesting bees (Sheffield et al., 2013). Ground nesting bees, (digger bees), nest in various soil conditions but mostly in well-drained sandy soils with sun exposure often in or very close to farm fields (Cane, 1991). The most common bees collected on watermelon fields in our study, tiny sweat bees Lasioglossum spp. , nests in sandy, loamy and clay soils in solitary, communal or social colonies depending on the species
(Gibbs, 2011). Most wild bees’ nesting habits are poorly understood or have never been studied so there is a lack of information on this topic. Cavity-nesting bees have much
157 different requirements since they excavate wood or use pre-existing rodent or insect holes and plant material as nests. Forest edges near fields provide much of the wood, dead and rotting plant material, snags and abandoned rodent holes needed by cavity nesting bees. Bumble bees, one of the most frequent and likely important pollinators of watermelon in our region, nest in tufts of grass, under sheds and hay bales, and in old rodent holes (Hatfield et al., 2012). Thus, maintaining semi-natural areas on the farm, especially woods and meadows, would enable these bees to nest closer to the farm field, making them more likely to visit a crop in bloom. Reducing disturbances at the soil level or below by incorporating no-till and avoiding herbicide spraying, mowing and driving over farm fields will protect wild bee nests. Other insects that pollinate watermelon and other crops often do not need nesting sites (i.e. syrphid flies) but may have other requirements such as host plants for larval stages (i.e. butterflies).
Exposed sandy soils in direct sunlight seen here in Charleston, South Carolina may provide nesting habitat for ground nesting bees in the field. A forested edge of the field may provide nesting habitat for cavity nesting bees.
Minimizing pesticide use. Pesticides, in combination with limited floral resources and increased pathogens and parasites, are linked to the sharp decline in recent years of domesticated and wild bees (Goulson et al., 2015). Herbicides and fungicides have sub-lethal effects on bees and their effects are more devastating when
158 used in combination with insecticides (Tsvetkov et al., 2017). Therefore, reducing agrochemical use on farm fields is essential to protecting pollinators for the future. Of course, some pesticides are more toxic than others and even some organic pesticides like
Spinosad are highly toxic to bees (Winfree, 2010). Systemic pesticides which became available in the 1990’s are especially toxic to pollinators because the chemical is taken up by all the plant tissues including the pollen and nectar. The most toxic pesticides for honey bees include organophosphates, neonicotinoids, pyrethroids, and the insect growth regulator novaluron (Park et al., 2015). Pesticide effects are much less understood for wild bees and are not included in the EPA pesticide registration process.
However, the neonicotinoids imadocloprid, clothianidin and thiamethoxam are highly toxic to bumble bees, blue orchard mason bees ( Osmia lignaria) and alfalfa leafcutter bees ( Megachile rotundata) . Bumble bees and solitary bees can be affected by lower concentrations of neonicitinoids than honey bees (Hopwood et al., 2016). Pollinators come into contact with pesticides directly or indirectly by foraging when spraying is occurring, by foraging on flowers from plants treated with systemic pesticides, by nesting in or near a field that has been sprayed, or by contacting residues on flowers or leaves after the application (Vaughan et al., 2015). Often growers heed to recommendations or pesticide labels that suggest avoiding spraying during periods of high honey bee activity or near their hives, but less notice is taken for wild bees
(Winfree, 2010). If pesticides are required, measures that can be taken to reduce non- target animals exposure to them include spraying in low wind conditions (<9mph), creating windbreaks and buffers between fields by planting stands of evergreen trees, avoiding formulations like dusts, wettable powders, micro-encapsulated broad- spectrum insecticides and flowable formulations, avoiding spraying during crop bloom,
159 spraying in the warmest weather possible, and spraying in the evening at least an hour after sunset when less pollinators are active. Reducing the need for pesticides by rotating crops, planting pest-resistant crop varieties, increasing habitat for predatory and parasitic insects and insectivorous birds, closely monitoring pest populations, and planting multiple crop types is also worth considering (Hopwood et al., 2016).
Wildflowers in agricultural areas attracts beneficial insects that can reduce the need for pesticide use by keeping pest populations in check. Some of the most common predatory and parasitic insects in wildflower strips in our study included vespid and sphecid wasps (L & middle) which consume other insects in their adult stage and drink nectar from flowers as a carbohydrate source and syrphid flies (R) which consume aphids and other insects in their larval stage and are nectar feeders as adults.
One way to address all three of these aspects of land management is to increase the amount of semi-natural habitat in the landscape (Kremen et al., 2004). This can be achieved by planting wildflowers in areas unsuitable for planting crops, letting part of the farm go fallow for a couple of years especially if it has significant pest issues, or retaining wooded areas as wildlife habitat. Organic farming practices, which include increased habitat heterogeneity, are expected to increase wild bee abundance and richness by 70% and 50%, respectively (Kennedy et al., 2013). These resulting multifunctional landscapes can enhance other ecosystem services such as soil fertility, pest regulation and carbon sequestration without diminishing crop yields (Kremen and
Miles, 2012). For more information on improving conditions for bees on farms, see https://xerces.org/pollinator-conservation/agriculture/.
160 Farmers can access multiple sources of funds and guidance for creating pollinator habitat on their farm. NRCS (Natural Resource Conservation Service) and (FSA) Farm
Service Agency provide federal funds and technical assistance through programs like
CRP (Conservation Reserve Program). In addition, Project Apis m is a non-profit organization that gives wildflower seed mixes and technical guidance to farmers through the Seeds for Bees program https://www.projectapism.org/apply-to-enroll.html.
4. Could wildflowers draw pollinators away from my crop or have other negative effects? Given that most pollinators in our region are generalists, meaning they forage on a wide variety of flowering plants, a legitimate question is whether incorporating other flowers onto a watermelon field would draw pollinators away or cause competition between the crop and other flowers for pollination. However, bees, flies, and even pollinating birds often forage on only one type or species of flower during their foraging bouts, ignoring other rewarding species (Waser, 1986). This behavior is called floral constancy, which Aristotle noted about honey bees in 350 BC: “On each expedition the bee does not fly from a flower of one kind to a flower of another, but flies from one violet, say, to another violet, and never meddles with another flower until it has got back to the hive" (Grant, 1950). Floral constancy is a desirable trait for crop pollinators because it reduces the possibility of different species of pollen mixing when the pollinator collects from multiple floral species (Waser, 1986).
161
American bumble bee ( Bombus pensylvanicus) females foraging on three flower species in watermelon fields ( Zinnia elegans/ Zinnia, Gaillardia pulchella/ Indian blanket and Citrullus lanatus/ Watermelon)
In a two-year study in Charleston, SC (2016 & 2018), we found that most watermelon pollinator species (62%) also foraged on at least one of the other flower species in watermelon fields, but most individuals of several species observed did not move between floral species during their foraging bouts when multiple flower species were available. This implies that individuals of the same species or colony (in social species) vary in their floral choice but tend to be specialists on those species. Of the pollinator species observed, bumble bees had the highest rate of instances where they moved between floral species, but bumble bees also had the fastest flower handling time and have been previously shown to be highly effective at pollinating watermelon flowers because of how much pollen they can deposit per visit (Campbell et al., 2018).
Therefore, their floral inconstancy may be outweighed by other qualities that make them efficient pollinators, including being some of the earliest visitors to watermelon when the flowers are most receptive to pollen receipt (Stanghellini et al., 2002).
Flowers with different forms (i.e. corolla length, petal shape, stigmatic surface area, tripping mechanisms, etc.) require pollinators to use different handling techniques to access pollen and nectar. This makes switching between floral species with different forms more energetically costly than staying constant to one species (Heinrich, 1976). In contrast, floral species with similar forms may require the same handling techniques,
162 allowing the pollinator to switch between species much more easily (Amaya-Marquez,
2009) . Therefore, choosing floral species for a wildflower strip or hedgerow with a wide range of flower shapes, sizes and colors may encourage pollinators to stick to one species as they forage in a watermelon field. By pollinators remaining true to one floral species, the crop is more likely to receive only pollen of its own kind which is linked to better reproduction in plants. Moreover, the risk of foreign pollen clogging up the female reproductive parts is much reduced (Waser, 1986).
Density of wildflowers and other flowering species on an agricultural field while the crop is in bloom may also play an important role in determining whether other flowering species compete with or facilitate crop pollination (Rathcke, 1983). Thus, adding wildflowers, hedgerows or reducing herbicide use on weedy flowers on a small scale near agricultural fields during the period when the crop is in bloom may be preferable to planting dense stands of co-flowering species. Additionally, choosing wildflowers or cover crops that flower before and after crop bloom but less during crop bloom would attract pollinators to the area before crop bloom, provide enough food sources to maintain healthy populations beyond crop bloom, and alleviate the potential for competition with the crop. Lastly, providing additional flowers on a perennial, long- term basis and including nesting resources may ensure that these farm enhancements support adjacent crop pollination instead of competing for pollinators (Morandin and
Kremen, 2013).
163
White clover ( Trifolium repens), Verbena ( Verbena hastata), and Watermelon (Citrullus lanatus) are examples of flowers with very different floral morphologies, i.e. amount of floral rewards, color, corolla shape and length to access nectar, and openness/ease of access). They are also from three different plant families (Fabaceae, Verbenaceae, Cucurbitaceae) which evolved with a different suite of pollinators. Pollinators learn how to handle each of these flower types differently to forage with the least amount of energy and species are adapted to certain floral morphologies.
In addition, there is much more evidence that implementing additional floral resources on a farm is beneficial to crop pollination than there is that floral enhancement has any negative effects. Blueberries, tomatoes and mangos are among many other crops that have shown higher pollinator visitation and crop yields when additional flowers are provided in the form of wildflower strips or hedgerows on farm fields (Haaland et al., 2011). These benefits stem from the additional pollination services that a more diverse community of pollinators provide, which a farm with more diverse flowers can support. In our study, watermelon flowers in fields with wildflowers tended to receive about the same number of visits as when there were no additional floral resources, but small native bees ( Lasioglossum spp.) visited watermelon flowers much more often when wildflowers were present. Thus, wildflowers are likely not competing for pollination services but simply adding to the diversity of food resources, attracting and maintaining a diverse pollinator community.
Overall, the behavior of watermelon pollinators on our fields supports recommendations and growing evidence for providing floral resources in agricultural areas to support and attract a diverse native pollinator community. A diverse pollinator
164 community, like the one observed in many of our watermelon fields, provides a more resilient and more stable pollination environment for watermelon and other pollinator- dependent crops than managed pollinators alone could provide (Brittain et al., 2013).
The benefits of resilience and stabilization to the crop pollination services as well as the inherent value of biodiversity arguably outweigh the possibility that bees could move between floral species.
165 166 Common Native Pollinators of Watermelon in South Carolina In this section I give an overview and visual guide to the 8 most frequent visitor groups to watermelon observed during my study. Ground-nesting bees Seventy percent of wild bees nest underground, including most of the watermelon pollinating bees in our region. They excavate tunnels and egg chambers in the soil where the larvae develop. The type and conditions of soil they use are dependent on species but many use well-drained sandy or loamy soils. To protect them: Reduce tilling or use no-till and reduce mulching and herbicide use. Drip- irrigation is preferable over flood irrigation or overhead spraying. Leave areas of bare ground on field edges and avoid driving over them. Many ground-nesting bees nest very close to the floral resource, and often in or near agricultural fields. Provide diverse floral resources before and after the crop bloom period. Tiny sweat bees ( Lasioglossum spp.: Halictidae): L. callidum, L. puteulanum, L. tamiamense Size: very small , 3.4 - 8 mm in length Color: grey-green metallic Sociality: ranges from solitary-primitively eusocial 17 species collected on SC watermelon fields Also forage on wildflowers and weeds Most frequent visitors to watermelon on many study fields, especially when wildflowers are also present
167
Medium sweat bees ( Halictus spp. : Halictidae) H. poeyi, H. rubicundus
Size: small-med Color: striped white/black abdomen Sociality: primitively eusocial 2 species collected on SC watermelon fields Also forage on wildflowers /weeds Very frequent in central SC watermelon fields pollinating watermelon, more commonly seen foraging on wildflowers in coastal SC
Blue-green sweat bees Agapostemon spp., Augochlorella aurata, Augochlora pura*
168
Size: small-medium Color: bright metallic green to green/blue, male Agapostemon have a striped yellow and black abdomen Sociality: solitary 5 species collected on SC watermelon fields Also forage on wildflowers/weeds Occasional watermelon visitor *A.pura is a cavity nester in rotting wood, but is in the same taxonomic group as these
Agapostemon sp. Augochlorini Augochlorini
Long-horned bees ( Melissodes spp. : Apidae) : Two-spotted long horned bee ( M. bimaculata) Common long horned bee (M. communis)
Size: medium Color: varies, M. bimaculata is all black except for whitish/yellowish hind legs, M. communis has distinctive white/black striping on abdomen Sociality: solitary 5 species collected on SC watermelon fields Also forage on wildflowers/weeds Very frequent in coastal and central SC watermelon fields
169 M. bimaculata ♀ M. bimaculata ♀
M. bimaculata ♂ M. communis ♀
Cavity-nesting Bees These bees have a wide range of nesting habits but either excavate their nests in soft wood or use pre-existing cavities and a variety of types of plant matter, mud or resin to construct brood cells. They require natural habitat near farms as nest sites and will forage varying distances to find food from there. Artificial nests such as wooden blocks with holes drilled in them allow for nesting of certain species with varying degrees of success.
To protect them: Natural habitat near farms, especially forest edges, should be protected. Dead plant material, brush piles, rotting wood, hollow stems and snags should be left untouched and collected near fields. Reduce tilling, mowing and other near-surface or sub-surface disturbance. Provide diverse floral resources before and after crop bloom.
Leafcutter bees ( Megachile spp. : Megachilidae) M. mendica, M. texana
Size: medium Color: varies, usually striped abdomen black/white, females typically have an abdomen that comes to a point like a teardrop, whereas males have a rounded abdomen Sociality: solitary 5 species collected on SC watermelon fields Also forage on wildflowers/weeds Frequent visitors of watermelon in coastal and central SC
170
Notes: specialized pollen collecting hairs (scopa) are on the underside of the abdomen in females; females usually use fresh leaves to line the cells of brood in old wood-boring beetle holes or other wood cavities; males are often territorial
Megachile sp. ♂ Megachile sp. ♀
Megachile sp. ♂ Megachile sp. ♀
Large carpenter bees ( Xylocopa spp. : Apidae) Eastern carpenter bee ( X. virginica) Southern carpenter bee (X. micans)
Size: large color: all black with shiny abdomen ( X.micans ), black head and shiny black abdomen with brown thorax (X. virginica ) Sociality: solitary 2 species collected on SC watermelon fields Also forage on wildflowers/weeds Frequent visitors of watermelon in coastal and central SC
Notes: nest in solid soft wood; males very territorial; distinguishable from bumble bees because of the shiny black abdomen whereas bumble bees have dense hair over their entire body X. micans X. micans
171 X. virginica
Bumble bees ( Bombus spp : Apidae) Common eastern bumble bee ( B. impatiens) Southern plains bumble bee ( B. fraternus) American bumble bee ( B. pensylvanicus) Brown-belted bumble bee ( B. griseocollis)
Size: large color: yellow and black in various color patterns, dense hairs cover almost every part of their body Sociality: primitively eusocial 4 species collected on SC watermelon fields Also forage on wildflowers/weeds Frequent visitors of watermelon in coastal and central SC
Notes: Bumble bees nest below, on or above the ground in various cavities including old rodent holes, tufts of large grasses, or hay bales. The American bumble bee ( Bombus pensylvanicus) is an International Union for Conservation of Nature (IUCN) vulnerable species, exhibiting alarming declines especially in its northeastern range (Bartomeus et al., 2013). The Southern plains bumble bee ( Bombus fraternus) is an IUCN endangered species, found in only 27% of its historic range with significant declines in its relative abundance (Colla et al., 2012). Habitat loss due to land conversion to intensive agriculture and pesticides are noted as the top two reasons for these species’ recent declines.
172 B. impatiens B. pensylvanicus ♀ B. fraternus ♀
B. impatiens B. griseocollis B. pensylvanicus ♀
B. fraternus ♂ B. pensylvanicus ♂
Other insects Other insects are less frequent watermelon pollinators, making up 2-7% of visits over 3 years of study on SC watermelon fields. They include skippers (Hesperiidae), butterflies, wasps, and flies but the most common are syrphid flies. Non-bee pollinators are an important part of the pollinator community and insect biodiversity, and some species larval or adult stages prey on insect pests in agricultural fields.
Syrphid flies (Syrphidae) Palpada spp., Toxomerus spp.
Size: medium Color: amber/golden stripes, distinguishable from bees because of large eyes that wrap around entire head, only 2 true wings and miniscule antennae Also forage on wildflowers/weeds Occasional visitors of watermelon in coastal and central SC
173
174 Photo Credit: All photos were taken by Mimi Jenkins and Merle Shepard Cover Art: Designed and Illustrated by Xing Guo Funding: This project was completed as part of M. Jenkins dissertation, funded by the Agricultural Society of South Carolina, Watermelon Promotion Board, and the Margaret H. Lloyd Smartstate Endowment
Two-spotted long horned bee / Melissodes bimaculata
Leafcutter bee/ Megachile sp.
Southern plains bumble bee/ Bombus fraternus
Blue-green sweat bee / Augochlorini
Tiny sweat bee/ Lasioglossum sp.
References:
Allen J, Wu KS, 2002. Modeling and Predicting of Future Urban Growth in the Charleston, South Carolina Area. Amaya-Marquez, M., 2009. Floral constancy in bees: a revision of theories and a comparison with other pollinators. Rev. Colomb. Entomol. 35, 206–216. Bartomeus, I., Ascher, J.S., Gibbs, J., Danforth, B.N., Wagner, D.L., Hedtke, S.M., Winfree, R., 2013. Historical changes in northeastern US bee pollinators related to shared ecological traits. Proc. Natl. Acad. Sci. 110, 4656–4660. https://doi.org/10.1073/PNAS.1218503110
175 Brittain, C., Kremen, C., Klein, A.-M., 2013. Biodiversity buffers pollination from changes in environmental conditions. Glob. Chang. Biol. 19, 540–547. https://doi.org/10.1111/gcb.12043 Campbell, J.W., Daniels, J.C., Ellis, J.D., 2018. Fruit Set and Single Visit Stigma Pollen Deposition by Managed Bumble Bees and Wild Bees in Citrullus lanatus (Cucurbitales: Cucurbitaceae). J. Econ. Entomol. 111, 989–992. https://doi.org/10.1093/jee/toy008 Cane JH, 1991. Soils of ground-nesting bees (Hymenoptera: Apoidea): texture, moisture, cell depth and climate. J. Kansas Entomol. Soc. 64, 406–413. Colla, S.R., Gadallah, F., Richardson, L., Wagner, D., Gall, L., 2012. Assessing declines of North American bumble bees (Bombus spp.) using museum specimens. Biodivers. Conserv. 21, 3585–3595. https://doi.org/10.1007/s10531-012-0383-2 Deguines, N., Julliard, R., de Flores, M., Fontaine, C., 2016. Functional homogenization of flower visitor communities with urbanization. Ecol. Evol. 6, 1967–1976. https://doi.org/10.1002/ece3.2009 Garibaldi, L.A., Carvalheiro, L.G., Leonhardt, S.D., Aizen, M.A., Blaauw, B.R., Isaacs, R., Kuhlmann, M., Kleijn, D., Klein, A.M., Kremen, C., Morandin, L., Scheper, J., Winfree, R., 2014. From research to action: enhancing crop yield through wild pollinators. Front. Ecol. Environ. 12, 439–447. https://doi.org/10.1890/130330 Gibbs, J., 2011. Revision of the metallic Lasioglossum (Dialictus) of eastern North America (Hymenoptera: Halictidae: Halictini)Revision of the metallic Lasioglossum (Dialictus) of eastern North America (Hymenoptera: Halictidae: Halictini). Zootaxa 3073, 1–216. Goulson D, Nicholls E, Botias C, Rotheray EL, 2015. Bee declines driven by combined stress from parasites, pesticides and lack of flowers. Science (80-. ). 347. Grant, V., 1950. The flower constancy of bees. Bot. Rev. 16, 379–398. https://doi.org/10.1007/BF02869992 Greenleaf, S.S., Williams, N.M., Winfree, R., Kremen, C., 2007. Bee foraging ranges and their relationship to body size. Oecologia 153, 589–596. https://doi.org/10.1007/s00442-007-0752-9 HAALAND, C., NAISBIT, R.E., BERSIER, L.-F., 2011. Sown wildflower strips for insect conservation: a review. Insect Conserv. Divers. 4, 60–80. https://doi.org/10.1111/j.1752-4598.2010.00098.x Hatfield, R., Jepsen, S., Lee-Mäder, E., Black, S., 2012. Conserving bumble bees: guidelines for creating and managing habitat for America’s declining pollinators. Heinrich, B., 1976. Bumblebee Foraging and the Economics of Sociality. Am. Sci. 64, 384–395. Hopwood J, Code A, Vaughan M, Biddinger D, Sheperd M, Black S, Mader E, Mazzacano C, 2016. How Neonicotinoids Can Kill Bees. Portland OR.
176 Intergovernmental Science ‐Policy Platform on Biodiversity and Ecosystem Services, 2016. Summary for policymakers of the assessment report of the Intergovernmental Science ‐Policy Platform on Biodiversity and Ecosystem Services on pollinators, pollination and food production. Bonn, Germany. Kennedy, C.M., Lonsdorf, E., Neel, M.C., Williams, N.M., Ricketts, T.H., Winfree, R., Bommarco, R., Brittain, C., Burley, A.L., Cariveau, D., Carvalheiro, L.G., Chacoff, N.P., Cunningham, S.A., Danforth, B.N., Dudenhöffer, J.-H., Elle, E., Gaines, H.R., Garibaldi, L.A., Gratton, C., Holzschuh, A., Isaacs, R., Javorek, S.K., Jha, S., Klein, A.M., Krewenka, K., Mandelik, Y., Mayfield, M.M., Morandin, L., Neame, L.A., Otieno, M., Park, M., Potts, S.G., Rundlöf, M., Saez, A., Steffan-Dewenter, I., Taki, H., Viana, B.F., Westphal, C., Wilson, J.K., Greenleaf, S.S., Kremen, C., 2013. A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecol. Lett. 16, 584–599. https://doi.org/10.1111/ele.12082 Klein, A.-M., Vaissière, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., Kremen, C., Tscharntke, T., 2006. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B Biol. Sci. 274, 303–313. https://doi.org/10.1098/rspb.2006.3721 Kremen, C., Merenlender, A.M., 2018. Landscapes that work for biodiversity and people. Science 362, eaau6020. https://doi.org/10.1126/science.aau6020 Kremen, C., Williams, N.M., Aizen, M.A., Gemmill-Herren, B., LeBuhn, G., Minckley, R., Packer, L., Potts, S.G., Roulston, T., Steffan-Dewenter, I., Vázquez, D.P., Winfree, R., Adams, L., Crone, E.E., Greenleaf, S.S., Keitt, T.H., Klein, A.-M., Regetz, J., Ricketts, T.H., 2007. Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. Ecol. Lett. 10, 299–314. https://doi.org/10.1111/j.1461-0248.2007.01018.x Kremen, C., Williams, N.M., Bugg, R.L., Fay, J.P., Thorp, R.W., 2004. The area requirements of an ecosystem service: crop pollination by native bee communities in California. Ecol. Lett. 7, 1109–1119. https://doi.org/10.1111/j.1461- 0248.2004.00662.x Kremen C, Chaplin-Kramer R, 2007. Insects as Providers of Ecosystem Services: Crop Pollination and Pest Control, in: Stewart, A.J.A., New, T.R. & Lewis, O.T. (Ed.), Insect Conservation Biology: Proceedings of the Royal Entomological Society ... - Royal Entomological Society of London. CABI Publishing, Wallingford, pp. 349– 382. Kremen C, Miles A, 2012. Ecosystem Services in Biologically Diversified versus Conventional Farming Systems: Benefits, Externalities, and Trade-Offs. Ecol. Soc. 17. Lee, K. V., Steinhauer, N., Rennich, K., Wilson, M.E., Tarpy, D.R., Caron, D.M., Rose, R., Delaplane, K.S., Baylis, K., Lengerich, E.J., Pettis, J., Skinner, J.A., Wilkes, J.T., Sagili, R., vanEngelsdorp, D., Partnership, for the B.I., 2015. A national survey of managed honey bee 2013–2014 annual colony losses in the USA. Apidologie 46, 292–305. https://doi.org/10.1007/s13592-015-0356-z
177 Matteson, K.C., Ascher, J.S., Langellotto, G.A., 2008. Bee Richness and Abundance in New York City Urban Gardens. Ann. Entomol. Soc. Am. 101, 140–150. https://doi.org/10.1603/0013-8746(2008)101[140:braain]2.0.co;2 Morandin, L.A., Kremen, C., 2013. Hedgerow restoration promotes pollinator populations and exports native bees to adjacent fields. Ecol. Appl. 23, 829–839. https://doi.org/10.1890/12-1051.1 Neumann, B., Vafeidis, A.T., Zimmermann, J., Nicholls, R.J., 2015. Future Coastal Population Growth and Exposure to Sea-Level Rise and Coastal Flooding - A Global Assessment. PLoS One 10, e0118571. https://doi.org/10.1371/journal.pone.0118571 Park, M., Danforth, B., Losey J, Biddinger D, Vaughan M, Dollar J, Agnello A, 2015. Wild pollinators of eastern apple orchards and how to conserve them. Potts, S.G., Biesmeijer, J.C., Kremen, C., N., 2010. Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. Rathcke, B., 1983. Competition and Facilitation Among Plants for Pollination, in: Real, L. (Ed.), Pollination Biology. Elsevier, p. 305-. Ricketts, T.H., Regetz, J., Steffan-Dewenter, I., Cunningham, S.A., Kremen, C., Bogdanski, A., Gemmill-Herren, B., Greenleaf, S.S., Klein, A.M., Mayfield, M.M., Morandin, L.A., Ochieng’, A., Viana, B.F., 2008. Landscape effects on crop pollination services: are there general patterns? Ecol. Lett. 11, 499–515. https://doi.org/10.1111/j.1461-0248.2008.01157.x Sheffield CS, Kevan PG, Pindar A, Packer L, 2013. Bee (Hymenoptera: Apoidea) diversity within apple orchards and old fields in the Annapolis Valley, Nova Scotia, Canada. Can. Entomol. 145, 94–114. Stanghellini, M.S., Ambrose, J.T., Schultheis, J.R., 2002. Diurnal activity, floral visitation and pollen deposition by honey bees and bumble bees on field-grown cucumber and watermelon. J. Apic. Res. 41, 27–34. https://doi.org/10.1080/00218839.2002.11101065 Tippett R, 2015. Population Growth in the Carolinas: Projected vs. Observed Trends [WWW Document]. Carolina Demogr. UNC Chapel HIll . URL https://demography.cpc.unc.edu/2015/12/08/population-growth-in-the-carolinas- projected-vs-observed-trends/ (accessed 3.18.19). Tscharntke, T., Klein, A.M., Kruess, A., Steffan-Dewenter, I., Thies, C., 2005. Landscape perspectives on agricultural intensification and biodiversity - ecosystem service management. Ecol. Lett. 8, 857–874. https://doi.org/10.1111/j.1461- 0248.2005.00782.x Tsvetkov, N., Samson-Robert, O., Sood, K., Patel, H.S., Malena, D.A., Gajiwala, P.H., Maciukiewicz, P., Fournier, V., Zayed, A., 2017. Chronic exposure to neonicotinoids reduces honey bee health near corn crops. Science 356, 1395–1397. https://doi.org/10.1126/science.aam7470 Vaughan M, Hopwood J, Lee-Mader E, Shepherd M, Kremen C, Stine A, Black S, 2015.
178 Farming for Bees: Guidelines for providing native bee habitat on farms. Portland OR. Vázquez, D.P., Morris, W.F., Jordano, P., 2005. Interaction frequency as a surrogate for the total effect of animal mutualists on plants. Ecol. Lett. 8, 1088–1094. https://doi.org/10.1111/j.1461-0248.2005.00810.x Waser, N.M., 1986. Flower Constancy: Definition, Cause, and Measurement. Am. Soc. Nat. 127, 593–603. Williams, N., Crone, E., T’ai, H., RL Minckley, Packer, L., Potts, S., 2010. Ecological and life-history traits predict bee species responses to environmental disturbances. Biol. Conserv. 10. Winfree, R., 2010. The conservation and restoration of wild bees. Ann. N. Y. Acad. Sci. 1195, 169–197. https://doi.org/10.1111/j.1749-6632.2010.05449.x Winfree, R., Bartomeus, I., Cariveau, D.P., 2011. Native Pollinators in Anthropogenic Habitats. Annu. Rev. Ecol. Evol. Syst. 42, 1–22. https://doi.org/10.1146/annurev- ecolsys-102710-145042 Winfree, R., Williams, N.M., Dushoff, J., Kremen, C., 2007. Native bees provide insurance against ongoing honey bee losses. Ecol. Lett. 10, 1105–1113. https://doi.org/10.1111/j.1461-0248.2007.01110.x
179