Floral Enhancement of Turfgrass Lawns for the Benefit of Bee Pollinators in Minneapolis, Minnesota a Thesis SUBMITTED to the FA

Floral Enhancement of Turfgrass Lawns for the Benefit of Bee Pollinators in

Minneapolis, Minnesota

A Thesis

SUBMITTED TO THE FACULTY OF

UNIVERSITY OF MINNESOTA

James Ithan Wolfin

IN PARTIAL FULFILLMENT OF THE REQUIREMENTS

FOR THE DEGREE OF

MASTER OF SCIENCE

Dr. Marla Spivak and Dr. Eric Watkins

January, 2020

Acknowledgements

I would like to thank everyone who helped me on this journey. I have been lucky to have two fantastic, supportive advisors, Drs. Marla Spivak and Eric Watkins, who have provided me with invaluable guidance, expertise, and, when needed, encouragement as I’ve worked on this project. The members of the Bee Lab and Turfgrass Science Lab have provided me with the tools to become a true bee expert and turfgrass scientist. I can say with absolute certainty that I would not be in this position without the expertise of Ian

Lane, Andrew Hollman, Zach Portman, Sam Bauer, Elaine Evans, Jon Trappe, and countless others in the Bee Lab and Turfgrass Science labs. I was fortunate enough to have the assistance of fantastic technicians, Rachel Urick and Maddie Bergum, who shared my passion for bees and conservation, and consistently exceeded my expectations with the quality of work they produced.

My parents, Steve and Madelyn Wolfin, have been my earliest teachers, my greatest cheerleaders, and have provided me the emotional support and encouragement

I’ve needed to succeed as a student, a professional, and as a man. My brother Michael is my best friend, my mentor, and has been and will continue to be an inspiration to me throughout my life. My friends from home, college, and graduate school have eased the burden that is graduate school, and I am forever grateful to them as they not only accept me and my peculiar love of bees, they even do their best to embrace my passion. Finally, shoutout my fantastic pets Lexi, Pookie, and Sami (Cat), and the constant smiles they bring to my face.

Dedication

I dedicate this work to my mother, who has provided me with the foundation needed to succeed every step of the way throughout my academic journey. From an early age, earlier than I can even remember, you’ve imparted so much wisdom onto me that set the foundation for my success. You taught me how to study, you taught me the value of diligence, and you’ve believed in me through all my successes and failures, even when I failed to believe in myself. You’re the first person I turn to when I need support, and the only person who can lift me up in times of doubt. While this is likely my last academic venture, it is the life lessons that I have learned from you that have carried me to this point, and that will continue to guide me every step of the way as I grow as a professional and as a man. This may mark the end of my academic career, but because of you, I will never stop being a student. Thank you.

Abstract

The turfgrass lawn is a common feature of urban and suburban communities, often accounting for the largest green spaces by area in these landscapes. Flowering species within turfgrass lawns have the potential to serve as a source of forage for bee pollinators in urban and suburban areas. We intentionally introduced low-growing flowers to turfgrass lawns to promote bee diversity and reduce inputs, while maintaining the traditional aesthetics and recreational uses associated with lawns. We compared bee communities on lawns with naturally-occurring blooms of Trifolium repens to bee communities on florally enhanced lawns that contained Prunella vulgaris ssp. lanceolata and Thymus serpyllum in addition to T. repens. T. repens supported both wild bee communities and A. mellifera colonies, as 56 species of bees were observed on T. repens, with A. mellifera as the most common species observed. We found that florally enhanced lawns supported more diverse bee communities than lawns with just T. repens.

Furthermore, the bee communities supported by florally enhanced lawns were significantly different from the bee communities supported by lawns containing just T. repens based on presence-absence (Jaccard’s dissimilarity index). Our research indicates that A. mellifera colonies and wild bee communities can be supported by allowing T. repens to bloom in turfgrass lawns, and that further steps to promote the conservation of bees can be taken by land managers by intentionally introducing low-growing flowers to lawns.

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Table of Contents

Acknowledgements ...... i Dedication ...... ii Abstract ...... iii Table of Contents ...... iv List of Tables ...... vi List of Figures ...... vii Chapter 1: Thesis introduction ...... 1 Importance of bees ...... 1 Overview of bee pollination ...... 1 Apis mellifera: Value in agriculture and stressors ...... 3 Wild bees: Value in agriculture and stressors ...... 4 Land use changes and habitat conversion ...... 6 Overview of land use changes and effects on bees ...... 6 Urbanization and urban conservation efforts ...... 8 The turf lawn and other green spaces ...... 11 Overview of the turf lawn and lawn inputs ...... 11 Pollinator conservation within urban landscapes and the turf lawn ...... 13 Candidates for floral enhancement within turf lawns ...... 15 The value of T. repens and potential for floral enhancement in turf lawns ...... 19 Chapter 2: Floral Enhancement of Turfgrass Lawns for the Benefit of Bee Pollinators in Minneapolis, Minnesota ...... 21 Introduction ...... 21 General Methods ...... 26 Study area ...... 26 Floral enhancements ...... 26 Floral selection ...... 27 Site preparation...... 28 Vegetation surveys ...... 29

Bee surveys on T. repens ...... 30 Bee surveys on clover-only vs. florally enhanced plots ...... 31 Bee identification ...... 32 Data analysis ...... 33 Parks with T. repens only ...... 33 Results ...... 36 Floral abundance in Minneapolis public parks ...... 36 Bee communities on T. repens ...... 36 Functional traits of bees on T. repens ...... 37 Predicting floral visitors on T. repens ...... 38 Bee species composition at paired parks ...... 38 Bees collected on Enhanced Vs Clover-only Parks ...... 39 Bees collected by host plant ...... 40 Discussion ...... 41 Clover-only parks...... 41 Florally enhanced parks ...... 42 Floral establishment...... 44 Conclusions...... 45 References ...... 68 Appendix A ...... 82

List of Tables

TABLE 1. LIST OF SITES WHERE BEE SPECIMENS WERE COLLECTED OFF OF T. REPENS BLOOMS WITHIN TURFGRASS LAWNS OF MINNEAPOLIS PUBLIC PARKS...... 47 TABLE 2 NATURALLY-OCCURRING WEEDY SPECIES OBSERVED WITHIN FLOWERING LAWNS. BEES WERE NOT COLLECTED OFF OF THESE SPECIES AS THEY WERE NOT OBSERVED IN HIGH ABUNDANCE ON THESE FLOWERS...... 48 TABLE 3. SPECIES LIST INCLUDING ABUNDANCE AND FUNCTIONAL TRAITS OF BEE SPECIMEN COLLECTED OFF OF T. REPENS BLOOMS IN TURFGRASS LAWNS OF PARKS IN MINNEAPOLIS, MINNESOTA. ORIGIN WAS DEFINED AS EITHER NATIVE (N) OR EXOTIC (E)...... 49 TABLE 4. SUMMARY OF RESULTS OF GENERALIZED LINEAR MIXED MODEL WITH BEE ABUNDANCE AS THE RESPONSE VARIABLE AND BEE TYPE (WILD OR A. MELLIFERA), CLOVER ABUNDANCE, JULIAN DATE, AND YEAR AS THE EXPLANATORY VARIABLES. AN INTERACTION BETWEEN BEE TYPE AND CLOVER ABUNDANCE WAS INCLUDED IN THE MODEL. SITE WAS INCLUDED AS A RANDOM EFFECT...... 52 TABLE 5. COMPARISON OF SLOPES FOR THE CHANGE IN BEE ABUNDANCE WITH INCREASING T. REPENS ABUNDANCE FOR A. MELLIFERA AND WILD BEES. LCL REPRESENTS THE LOWER CONFIDENCE LIMIT, AND UCL REPRESENTS THE UPPER CONFIDENCE LIMIT, ACCORDING TO A 95% CONFIDENCE INTERVAL...... 53 TABLE 6. BEE SPECIES COLLECTED OFF OF FLOWERING LAWNS AT PAIRED PARKS IN MINNEAPOLIS, MINNESOTA BETWEEN 2016 AND 2018. SPECIES IN BOLD WERE ONLY COLLECTED AT FLORALLY ENHANCED PARKS. AN ASTERISK (*) INDICATES SPECIES THAT WERE COLLECTED ONLY OFF OF P. VULGARIS, A CARROT (^) INDICATES SPECIES THAT WERE COLLECTED ONLY OFF OF T. SERPYLLUM, AND A PLUS SIGN (+) INDICATES SPECIES THAT WERE COLLECTED OFF OF BOTH P. VULGARIS AND T. SERPYLLUM, BUT NOT T. REPENS...... 54

List of Figures

FIGURE 1. ARCGIS-MAP OF MINNEAPOLIS, MINNESOTA AND SURROUNDING AREAS DEPICTING SITE LOCATIONS (THUMBNAILS). BEES WERE COLLECTED OFF OF T. REPENS INFLORESCENCES WITHIN TURFGRASS LAWNS OF PUBLIC PARKS. GREEN PINS REPRESENT PAIRED FLORALLY-ENHANCED PARKS, BLUE PINS REPRESENT PAIRED CLOVER-ONLY PARKS, AND YELLOW PINS REPRESENT ADDITIONAL CLOVER-ONLY PARKS...... ERROR! BOOKMARK NOT DEFINED. FIGURE 2. CANDIDATES FOR FLORAL ENHANCEMENT FOR TURFGRASS LAWNS. TOP ROW (LEFT TO RIGHT) TRIFOLIUM REPENS, PRUNELLA VULGARIS, THYMUS SERPYLLUM. BOTTOM ROW (LEFT TO RIGHT) COREOPSIS LANCEOLATA, SYMPHIOTRICHUM LATERIFLORUM. ....ERROR! BOOKMARK NOT DEFINED. FIGURE 3. MEAN (+/- SE) ABUNDANCE OF LAWN INFLORESCENCES OBSERVED WITHIN FLOWERING LAWNS IN MINNEAPOLIS, MINNESOTA IN 2018. FLOWERS WERE COUNTED ALONG A THIRTY METER, FIXED TRANSECT, IMMEDIATELY FOLLOWING BEE SURVEYS ALONG THE SAME TRANSECT LINE. DATES ABOVE EACH BAR INDICATE THE BLOOM PERIOD FOR EACH SPECIES IN 2018. ..ERROR! BOOKMARK NOT DEFINED. FIGURE 4. SPECIES ACCUMULATION CURVE FOR BEES COLLECTED OFF OF T. REPENS AT MINNEAPOLIS PUBLIC PARKS. 56 BEE SPECIES WERE COLLECTED IN TOTAL, AND BOOTSTRAPPING SUGGESTS THAT 64 BEE SPECIES MAY BE PRESENT WITHIN THIS COMMUNITY...... ERROR! BOOKMARK NOT DEFINED. FIGURE 5. BEE ABUNDANCE ON T. REPENS BLOOMS WITHIN MINNEAPOLIS PARKS THROUGHOUT THE GROWING SEASON, SORTED BY JULIAN DATE...... 61 FIGURE 6. LINEAR REGRESSION DEPICTING THE RELATIONSHIP BETWEEN BEE ABUNDANCE AND T. REPENS ABUNDANCE IN TURFGRASS LAWNS OF 16 PUBLIC PARKS IN MINNEAPOLIS, MINNESOTA. THE BLACK LINE REPRESENTS THE RELATIONSHIP FOR A. MELLIFERA, AND THE GRAY LINE REPRESENTS THE RELATIONSHIP FOR WILD BEES. THE SHADED AREA AROUND EACH LINE DEPICTS CONFIDENCE INTERVALS...... 62 FIGURE 7. SPECIES ACCUMULATION CURVE FOR BEES COLLECTED AT PAIRED PARKS IN MINNEAPOLIS. 53 BEE SPECIES WERE COLLECTED IN TOTAL, AND BOOTSTRAPPING SUGGESTS THAT 61 BEE SPECIES MAY BE PRESENT WITHIN THIS COMMUNITY...... 63 FIGURE 8. EXPONENTIAL SHANNON'S INDEX OF ENTROPY AT CLOVER- ONLY AND FLORALLY ENHANCED PARKS IN MINNEAPOLIS, MINNESOTA, 2016-2018. FLORALLY ENHANCED PARKS EXHIBITED GREATER DIVERSITY (P= 0.046) THAN CLOVER-ONLY PARKS...... 64

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FIGURE 9. CHANGE IN THE EXPONENTIAL SHANNON'S INDEX OF ENTROPY AT ENHANCED AND CLOVER-ONLY PARKS BETWEEN 2016 AND 2018. PARKS THAT WERE FLORALLY ENHANCED EXHIBITED A GREATER INCREASE IN DIVERSITY (P=0.038) THAN PARKS THAT REMAINED CLOVER-ONLY DURING THIS TIME FRAME...... 65 FIGURE 10. NON-METRIC MULTIDIMENSIONAL SCALING ORDINATION OF THE COMMUNITY COMPOSITION OF BEES COLLECTED AT FLORALLY ENHANCED AND CLOVER-ONLY PARK IN MINNEAPOLIS, MINNESOTA, 2017-2018, ACCORDING TO THE MORISITA-HORN INDEX ...... 66 FIGURE 11. NON-METRIC MULTIDIMENSIONAL SCALING ORDINATION OF THE COMMUNITY COMPOSITION OF BEES COLLECTED FROM ENHANCED AND CLOVER-ONLY PARKS IN MINNEAPOLIS MINNESOTA, 2017-2018, ACCORDING TO THE JACCARD DISSIMILARITY INDEX...... 67

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Chapter 1: Thesis introduction

Importance of bees

Overview of bee pollination

Bees are a highly diverse group of insect pollinators that are considered essential contributors to modern ecosystems, primarily due to their role as pollinators of angiosperms (flowering plants). It is estimated that out of the 352,000 species of angiosperms present worldwide, 308,006 benefit from animals transferring pollen to conspecifics (Ollerton et al. 2011). Bees transitioned from a carnivorous diet to a florivorous diet in the late cretaceous period, about 150 million years ago, during which the primary source of carbohydrates comes from floral nectar and their primary source of protein and lipids comes from floral pollen. Along with this shift in diet other novel adaptations arose like the presence of branched body hairs, and in some cases scopae or corbiculae, which helped bees collect pollen. Bees may also exhibit specialized behaviors like sonication to aid in dislodging pollen from the anthers of flowers, and adding nectar to pollen to create a pellet that is easier to transport (Thorp 1979).

Angiosperm pollination by bees laid the foundation for a co-evolutionary, mutualistic relationship that allowed for the adaptive radiation of both groups (Willmer 2011).

Current surveys of global bee diversity have described nine families of bees and estimates that there are upwards of 22,000 bee species worldwide (Goulson et al. 2015;

Michener et al. 1994). A survey of bees in the north central United States estimated that there are at least 325 wild bee species present in the state of Minnesota (Wolf and Ascher

2008). More recent work at the insect museum at the University of Minnesota has estimated that there have been at least 400 bee species recorded in the state of Minnesota over the last 100 years (unpublished data). Maintaining pollinator diversity is critical to plant health, as numerous studies have found that bee diversity is highly correlated with plant diversity (Fontaine et al. 2005; Memmott et al. 2004; Potts et al. 2010).

The value of bees has been demonstrated through their role in modern agriculture, as many crops are highly dependent on bee pollination. Although some crops (corn, wheat) achieve pollination entirely independent of insect pollination, others, such as apple, blueberry, tomato, and almond are either entirely dependent on insect pollination or receive a yield benefit from pollinator visitation (Calderone 2012; Garratt et al. 2014).

Furthermore, it has been found that fruit quality may increase when insect pollinators are present (Garratt et al. 2014).

It is estimated that 35% of agricultural production depends on animal pollination to some extent, with insect pollination of directly dependent crops accounting for an ecosystem service valued at over $15 billion annually in the United States (Calderone et al. 2012). Bee pollination of indirectly dependent crops (crops where bees are required to create seeds) is valued at an additional $12 billion per year in the United States (Klein et al. 2007). A worldwide evaluation of the economic value of insect pollination estimated a value of €153 billion, or nearly $200 billion (Gallai et al. 2009). The value of insect pollination in agriculture is reinforced when considering the diversity of crops that benefit from insect pollination. A study of global food crop pollination (Klein et al.

2007) found that 87 out of 115 of the leading food crops worldwide are dependent on animal pollination, of which insect pollination by bees is a primary contributor.

Apis mellifera: Value in agriculture and stressors

Apis mellifera (European honey bee) is a highly-studied species with well- documented contributions to pollination within agriculture. Much of this is due to the practice of commercial beekeeping, where beekeepers maintain stocks of managed A. mellifera colonies and transport them locally, regionally, and even across the country to coincide with the major blooming periods of agricultural crops. A. mellifera is considered the most economically valuable species of pollinators worldwide, especially in monocultures (McGregor 1976; Watanabe 1994). Yields of specific fruits, nuts, and seed crops have been found to decrease in excess of 90% in the absence of A. mellifera

(Southwick and Southwick 1992).

A. mellifera has become engrained as a critical component of global agriculture and food security, and as such it is important that we monitor the health and population status of these insects. In recent years, A. mellifera health has become a topic of increasing concern, specifically after the onset of Colony Collapse Disorder (CCD). This problem was first described in 2006, and is defined as the inexplicable, sudden loss of honey bee workers in a colony, a phenomenon that, according to surveys, affected 24% of beekeeping operations between 2006 and 2007 (vanEngelsdorp et al. 2007; Oldroyd

2007). The cause of CCD could not be attributed to one particular stressor. By 2016, a survey of annual winter A. mellifera mortality estimated that beekeepers were still losing

29.5% of their bee colonies, with 59% of beekeepers responding that this rate of loss was higher than what they deem acceptable (Kulhanek et al. 2017). This decline in the population status and productivity of A. mellifera is now believed to be associated with several factors including the presence of pests and pathogens within honey bee colonies, the use of broad-spectrum pesticides, and changes in land use practices that reduce forage availability (Breeze et al. 2014; Chen et al. 2004; Oldroyd 2007; Potts et al. 2010;

Rosenkranz et al. 2010). Declines in honey bee health and productivity, coupled with a four-fold rise in agricultural production of crops that require animal pollination poses a serious risk to modern agriculture and global food security (Aizen and Harder 2009).

Wild bees: Value in agriculture and stressors

Declines in the health and population status of A. mellifera in the U.S. and Europe have led to increased concern for the status of wild bees. Improving the status of wild bee populations may allow for a reduced dependence on A. mellifera in agricultural and wild plant pollination. Furthermore, wild bees have been found to be more efficient pollinators of certain crop species and have the ability to improve crop yields regardless of the presence of A. mellifera (Parker et al. 1987; Torchio 1990; Mallinger and Gratton

2015). The ability to manage A. mellifera colonies facilitates the study of their life- history traits and behaviors. In contrast, it is much more difficult to study the natural history of wild bees, and it is difficult to assess the value of wild bees due to their wide range of behaviors and nesting strategies. Despite difficulties in measuring the pollination services and population numbers of wild bees, an estimate of the value of wild

4 bee pollination between 2001 and 2003 valued this ecosystem service to be at least $3.66 billion annually in the United States (Losey and Vaughan 2006; Klein et al. 2007).

Increased interest in the pollination services of wild bees has led to attempts to measure their populations and describe factors affecting their health. For example, the most well-studied wild bees are bumble bees (Bombus spp.), some of which are managed commercially. Studies of bumble bees in Europe have found ongoing decreases in diversity, including in the UK where 10 of 16 non-parasitic bumble bee species are believed to be in decline (Goulson et al. 2008; Williams and Osborne 2009). In the

United States, a comparison of current and historical distributions of bumble bee species showed that many have been experiencing declines in their abundance and geographic range between 1990 and 2010 (Cameron et al. 2011).

Many of the factors that have led to declines in the health and population status of A. mellifera have similar negative effects on wild bees. Widespread applications of broad- spectrum pesticides have been shown to cause mass die-offs of wild bees (Kevan 1975).

For example, a study of the effect of fenitrothion (a phosphorothioate insecticide) on wild bees and bumble bees (Brittain et al. 2010) found that pesticide exposure can result in reduced diversity of wild bees, including bumble bees. There is also evidence to suggest that A. mellifera can increase the risk of the spread of parasites and pathogens to wild bees. Mazzei et al. 2014 found that deformed wing virus (DWV), a common A. mellifera disease, can be spread by A. mellifera to pollen loads in flowers, and subsequently infect the wild bee species Osmia cornuta via horizontal transmission of the pathogen.

Furthermore, lab results from Graystock et al. (2015) suggest that flowers that serve as 5 forage for bumble bees and A. mellifera can serve as hotspots for the transmission of pollinator parasites between bumble bees and A. mellifera. While A. mellifera may be able to indirectly transfer diseases and pathogens to wild bees, there is no evidence to suggest that A. mellifera colonies have caused declines in wild bee populations.

Increased diversity and abundance of flowering plants may improve access to forage and potentially reduce competition for resources between A. mellifera and wild bee species.

Reduced competition between A. mellifera and wild bee populations would likely mitigate the transfer of A. mellifera diseases to wild bees, as there would be less overlap while foraging.

Land use changes and habitat conversion

Overview of land use changes and effects on bees

Land-use changes, including the conversion of natural lands like prairies, grasslands, and forests to urban and agricultural lands, can result in the loss, fragmentation, or degradation of bee habitat and forage (Goulson et al. 2015). Declines in natural habitats have been noted in North America since the early 19th century (Samson and Knopf 1994), and have been associated with major contractions of bee populations (Goulson et al.

2008). Conversions of natural lands to either agricultural or urban lands have been shown to increase both pesticide application loads (Kevan 1997) and the spread of pathogens among bees (Neumann and Carreck 2010). For these reasons, land-use changes are often considered the primary factor driving bee declines (Brown and Paxton

2009; Potts et al. 2010) habitat suitability for honey bees and wild bees (Holzschuh et al. 6

2010; Otto et al. 2016). The negative effects of habitat loss and fragmentation are further displayed when considering the consequences that these stressors can have on pollination.

Ricketts et al. (2008) found that when there is a greater distance between natural or semi- natural habitats and cropping systems that require pollination, visitation rates and pollinator richness at the crop site experience a significant decline.

One of the primary ways in which habitat degradation can negatively affect bees is by reducing access to forage and nesting resources (Potts et al. 2010). Forage access is tied directly to the abundance and diversity of flowers present in the landscape, as flowers provide protein-rich pollen and carbohydrates from nectar that bees require to sustain life.

The abundance and diversity of flowers has declined across the world; for instance, in the

United Kingdom, where 97% of florally-rich grasslands were lost in the 20th century

(Goulson et al. 2015; Samson and Knopf 2003). This loss of flora was found to contribute to range contractions in many wild bee species. A study in the UK found evidence that 76% of the forage plants used by bumble bees experienced a decline in abundance between 1978 and 1998 (Carvell et al. 2006). Similar losses of grasslands have occurred in the United States, where 55 grassland prairie plants are listed as endangered, and another 728 species are viewed as candidates for listing (Samson and

Knopf 1993). The loss of high-quality habitat and forage has been of significant concern in Minnesota. According to the Minnesota Department of Natural Resources, in 1908

Minnesota had more than 18 million acres of prairie, or 1/3 of the state by area, however less than 1% of this land remains as native prairie today.

Agricultural intensification over the last 50 years has been identified as one of the primary contributors to habitat loss and habitat degradation for A. mellifera and wild bees worldwide, including in North America (vanEngelsdorp et al. 2008; Potts et al. 2010;

Cameron et al. 2011). Agricultural intensification is defined by large, high-input monoculture farms with simple crop rotation systems. While lands subject to agricultural intensification are high in productivity, they also reduce the proportion of grasslands and associated flowers that exist within a landscape (Herzog et al. 2006). Agricultural intensification in Europe has resulted in alterations to farming landscapes that have been associated with losses in farmland biodiversity (Robinson and Sutherland 2002). A study of bee diversity within mass flowering crops in Europe between 2011 and 2012 found that the densities of bumblebees, solitary bees, and A. mellifera were all negatively correlated with increased cover of mass flowering crops (Holzshuh et al. 2016).

Furthermore, there is evidence to suggest that the negative effects of agricultural intensification are more prominent for wild bees. A study of floral use in western France found that A. mellifera were prominent within mass-flowering cropping systems, while wild bees were more strongly associated with semi-natural habitats that could be found near the farms (Rollin et al. 2013).

Urbanization and urban conservation efforts

Urbanization, the conversion of land for urban land uses including commercial, industrial, and residential needs, is another form of land conversion that can greatly alter a landscape (Brown et al. 2005). A study tracking demographic trends in the United

States found that while urban areas only accounted for a small percent of land use in the

United States (6.6% as of 1997), they were experiencing a rapid increase in land cover

(Brown et al. 2005). Estimates suggest that nearly 80% of the United States population lived in or near cities as of 2005, and that urban land cover could climb as high as 9.2% by 2025 (Alig et al. 2004; McKinney 2005).

As urbanization becomes more common it is increasingly important to consider how to can best manage these lands for conservation purposes. Urbanization can alter ecosystem structure in several ways, including through habitat fragmentation, heterogeneity, loss and degradation, the introduction of new species, and alterations of nutrient levels (Kowarik 2011). While it is generally agreed that urbanization alters biodiversity, the full effects of urbanization on biodiversity are not fully understood.

Some studies indicate that urbanization may be beneficial for biodiversity, as areas with low to moderate human development tend to have high species richness (McKinney

2002); this has been shown in many insect groups including bumblebees, butterflies, and ants (Pawlikowski and Pokorniecka 1990; Nuhn and Wright 1979). A meta-analysis documenting the effects of urbanization on bees found that responses to urbanization varied by bee type. A trend was observed such that overall species richness decreased with increasing urbanization, however, cavity nesters and some floral specialists benefitted from urbanization (Hernandez et al. 2009). Banaszak-Cibicka and Zmihorski

(2012) determined that urbanization can filter the bee communities that are present, specifically favoring small-bodied, late-season bees.

Contrasting studies suggest that while urbanization and mild disturbance may increase species richness, this is only seen at the local diversity scale, with the same species benefitting from these land use changes across landscapes. A study of the effects of urbanization on wildlife in the United states found that urbanization creates homogenous landscapes that endanger more species than any other human land conversion (Czech et al. 2000). One factor contributing to this loss of species in urban landscapes is the replacement of native species with non-native species. Studies have shown that urbanization can increase the prevalence of non-native insects, birds, and plants, while reducing the number of native species of these taxa (Kowarik 2011; Blair and Launer 1997). Furthermore, unlike other natural land conversions (i.e. fire), urbanization tends to be permanent, such that ecological succession cannot occur in these areas to restore populations of native species that once existed in these areas (Stein et al.

2000). Ahrne et al. (2009) suggested that the area surrounding an urban landscape can significantly influence bee diversity, with surrounding impervious surface negatively correlated with bee diversity. Bates et al. (2011) evaluated the value of urban and suburban areas by comparing bee community composition across a gradient of landscapes ranging from urban to rural and found that while urban and suburban areas do have the capacity to support diverse pollinator communities, similar rural habitats were found to support greater bee abundance and diversity.

It is clear that urban areas are increasing in prominence, and it is therefore important to consider bee conservation within these areas. One strategy utilized in urban areas to promote conservation is to preserve as much remnant natural habitat as possible. These

10 natural remnants have increased species richness returns with increasing size, however it is uncommon for land managers and other public officials to allow this pre-existing vegetation to persist in urban development (Mckinney 2002; Wasowski and Wasowski

2000). A meta-analysis conducted by Beninde et al. (2015) provided additional evidence that increased site size and connectivity promotes urban conservation. They determined that sites greater than 50 ha can prevent the loss of species that are limited by patch size, and corridors can promote movement between patches. The authors also concluded that heterogenic vegetation structure within cities promotes biodiversity in urban areas by reducing the homogenization of species. Urban restoration projects, where developed communities install native plants in urban ecosystems, have become increasingly popular as a conservation strategy. Majer (1997) found that urban communities that allow natural plant succession to take place experienced an increase in arthropod diversity.

The turf lawn and other green spaces

Overview of the turf lawn and lawn inputs

A common feature of urban and suburban landscapes is the turf lawn. Turfgrass serves as the most prominent irrigated crop in the continental United States, accounting for nearly 2% of land cover (127,962 km2), which is greater than three times the area covered by irrigated corn (Milesi et al. 2005). Well-managed and properly maintained turf lawns can provide a number of benefits including serving as a recreational surface, carbon sequestration, and preventing soil erosion. While these ecosystem services provided by the turf lawn are valuable, a poorly managed or over-managed turf lawn can

11 be environmentally costly. Lawn inputs include the cultural practices of mowing, irrigation, and fertilizing; these are all practices used to maintain the quality of the lawn.

Lawn inputs often produce an aesthetically pleasing lawn, but each of these practices carry their own environmental consequences.

Mowing causes harm to the environment in the form of air pollutants released during each mowing event. An EPA study found that lawn and garden equipment is responsible for the emission of 26.7 million tons of pollutants in the United States annually, with lawn mowers serving as the most common piece of equipment utilized by land managers

(Banks and McConell 2015). The environmental harm of mowing can be mitigated by planting turfgrass species with a slow rate of growth, like fine fescues (Festuca sp.) and allowing for higher mowing heights. Christians et al. (2011) suggests that taller mowing heights can further benefit the environment by increasing the leaf area of the plant, which allows for an increased rate of photosynthesis.

Irrigation of turf lawns may cause environmental harm from a water conservation standpoint, and through runoff, where excess nutrients may be carried to nearby bodies of water, polluting these areas and causing algal blooms. Haith and Andre (2000) estimate that 400 cubic miles of water enters oceans annually as a result of runoff from turf. The ecological costs of irrigation are further displayed when combined with poor fertilizer practices. When nitrogen and phosphorus are applied to nutrient-sufficient soils, these nutrients may be carried to nearby bodies of water, causing algal blooms that diminish water quality (Ryther and Dunstan 1971). Turfgrass management plans suggest using low-input turfgrass species to create more sustainable lawns. Turfgrass species selection

12 can reduce the amount of irrigation applied to a turf lawn by selecting species with a low rate of water use. Aronson et al. (1987) found that, on average, fine fescue grasses have lower water use rates than Kentucky bluegrass cultivars, reducing the amount of water that needs to be applied to the fescues.

Pollinator conservation within urban landscapes and the turf lawn

Green spaces within urban areas have been shown to support diverse bee communities. One example includes urban green roofs, or roofs covered with vegetation, that have been found to promote diverse arrays of insects, including pollinators

(Brenneisen 2003). A study of urban bee diversity on green roofs throughout Canada found that vegetation on green roofs supported 79 species of bees, including 74 native species. Further studies on the viability of green roofs have shown that the value of green roofs as habitat for wild bees varies based on the diversity of floral resources provided.

Kratschmer et al. (2018) categorically ranked forage availability on green roofs in

Vienna, Austria from “very low” to “very high” across five categories. It was found that wild bee abundance and species richness increased at each increasing stage of forage availability.

Another example includes urban lawns, which could support pollinators by allowing flowering vegetation to persist in turf. Typically, turf lawns are managed to promote uniformity, where an ideal turf stand will consist of only turfgrasses. Data from Hugie et al. (2012) found that consumers prefer a lawn free of flowering species, as flowers within the turfgrass are considered a nuisance, or a “weed”, disrupting up the aesthetics of the

13 lawn. Under this management, turf lawns do not provide value in the form of forage to pollinators, as uniform stands of turfgrass do not provide rewards to pollinators in the form of nectar and pollen. In Paris, France, lawn management strategies have been altered to improve the value of turf lawns to pollinators. These lawns follow a

‘differential management’ program that creates favorable conditions for wild plants, reduces weeding frequency, and reduces mowing frequency. Shwartz et al. (2013) found that species richness of pollinator in lawns was positively correlated with lawn cover on turf lawns that utilized this differential management program.

Lawns with a mixture of turfgrass and naturally-occurring flowering species have been shown to support diverse bee communities. A study of bee communities in 17 suburban yards in Springfield, Massachusetts (Lerman and Milam 2016) found that lawns that were not treated with herbicides contained spontaneous (not planted) wild flowers that supported 111 bee species. The majority of the bees collected were native to North

America, solitary, and nested in the soil. Trifolium repens (Dutch white clover) and

Taraxacum officinale (dandelion) were the two most abundant lawn flowers observed in these lawns. A similar study in Lexington, Kentucky (Larson et al. 2014) aimed to describe the bee communities on T. repens and T. officinale and found that the two flowers supported 37 unique bee species suburban, with 21 bee species collected off of T. repens, and 25 species collected off of T. officinale.

While several studies have looked at the value of urban green spaces for bees, or the value of naturally-occurring lawn flowers for bees, few studies have explored the potential of intentionally managing lawn areas for bees. Lerman et al. (2018) found that

14 a “lazy lawnmower”, or reducing the frequency of mowing, can increase the abundance of flowers available to bees. They found mixed results regarding mowing frequency and bee diversity, as the lawns mowed most frequently were found to support the greatest bee species richness, but lawns with an intermediate frequency of mowing were found to support the greatest bee abundance. The authors determined that the increased species richness observed in lawns mowed most frequently was likely due to the presence of singleton species. Furthermore, the high abundance of bees observed in the intermediate mowing regime was due to the increased presence of common bees.

Candidates for floral enhancement within turf lawns

Inclusion of T. repens, Dutch white clover, with turfgrass has been proposed as a way of increasing habitat forage in urban areas, while improving the sustainability of the lawn. Studies have found that pre-seeding mechanical disruption strategies and timing of planting can promote the establishment of T. repens, and other low growing floral species in both warm-season and cool-season turfgrasses (McCurdy et al. 2013; Sparks et al.

2015; Lane et al. 2016). T repens is a perennial flower native to Europe that was initially introduced to turf lawns for its value in nitrogen fixation. In addition to its contribution to overall lawn health (Ledgard and Steele 1992; McNeill and Wood 1990; Sincik and

Acikgoz 2007; McCurdy et al. 2013), the value of T. repens to pollinators has been noted in various studies (McCurdy et al. 2013; Larson et al. 2014; Lerman and Milam 2016;

Lerman et al. 2018). A study detailing forage use by bees in 63 neighborhoods in

Chicago, Illinois found that T. repens was the most common plant visited by pollinators

(Lowenstein et al. 2018). A similar study found that T. repens was the most common forb utilized by two pollen generalist bee species throughout Canada, accounting for nearly 7% of all pollen collected off of bees (MacIvor et al. 2013). Floral rewards obtained from T. repens are highly nutritious, with an average pollen protein content of

35.4% with a volume of 4.3 µl per inflorescence, and an average nectar sugar content of average 42% sugar with an average volume of 0.1 µl per inflorescence (Roulston et al.

2000; Weaver 1965).

The shape and size of T. repens inflorescences allow a diverse community of bees to access its pollen and nectar. T. repens inflorescences consist of a collection of lance-like white petals that form a rounded shape when viewed together (Error! Reference source not found.). The floral rewards can be accessed by both large and small pollinators, as smaller pollinators use individual petals as a landing pad, while larger pollinators land on a collection of petals. T. repens blooms from late spring through early fall, at a height of

5-35 cm (Rakocevic et al. 2000), depending on mowing frequency.

Prunella vulgaris var. lanceolata is another candidate well suited for inclusion in flowering lawns. Lane et al. (2016) found that P. vulgaris can be established in a lawn via overseeding, and this species has been noted for its value to pollinators, including bees (NRCS 2012). Recommended management strategies to promote the establishment of P. vulgaris include pre-seeding disruption of turfgrass through scalping and core aeration, and planting in the fall as a dormant seeding (Lane et al, 2016). P. vulgaris var. lanceolata is a perennial flower native to North America, including Minnesota. Two varieties of P. vulgaris have been found in Minnesota--Prunella vulgaris var. lanceolata

16 and Prunella vulgaris var. vulgaris; however only the former is considered to be native to

Minnesota. P. vulgaris var. lanceolata has slightly smaller vegetation than P. vulgaris var. vulgaris. Previous trials with P. vulgaris have found that this plant is well adapted to a lawn setting. Overseeded P. vulgaris has been found to establish and bloom in the first year after planting, and continue to persist in lawns in subsequent years (Lane 2019b.

The same study showed that this plant is able to survive in both sandy soils, and clay/loam soils. P. vulgaris can establish and bloom in either partial shade or full sun.

Once in bloom, P. vulgaris flowers are displayed as part of a spike-shaped inflorescence.

Flowers are purple and have a long corolla (Error! Reference source not found.), which generally lends itself well to larger pollinators with longer tongues. The flowers of P. vulgaris persist from mid-spring through mid-late summer.

Lane (2019b) also proposed Thymus serpyllum as a candidate for inclusion in flowering lawns due to its ability to bloom at low heights, and the value it provides to pollinators. While T. serpyllum has been viewed as a floral species best-adapted for sandy, well drained soils, Lane (2019b) found that T. serpyllum can be established in a lawn setting in a variety of soil types. T. serpyllum is a perennial flower native to

Northern Europe that has become a common form of alternative ground cover in many home yards and gardens. T. serpyllum is a full sun plant that thrives in sandy, dry soils.

The drought tolerance of T. serpyllum makes it a low-maintenance plant, as once it is established in the soil it has low irrigation requirements, though it can also survive in soils with finer particles that retain more water. Vegetation for this flower may be observed in the first year after planting, but blooms are not likely to be observed until

17 year 2-3 after planting. T. serpyllum can bloom at heights below three inches, and the showy, open blooms are accessible to small bees with short tongues. T. serpyllum blooms display a deep pink color that has been shown to be attractive to pollinators

(Error! Reference source not found.). Blooms of T. serpyllum may be observed late in the bee foraging season, starting in the mid-summer and persisting through the early fall.

Symphiotrichum lateriflorum (Calico aster) is capable of blooming at heights that are amenable with conventional mowing regimes (Lane, unpublished data). The value of S. lateriflorum to pollinators has not been formally analyzed, however, the closely related

Symphiotrichum lanceolatum has been noted as a species that is commonly visited by bumble bees (Chmielewski and Semple 2001). S. lateriflorum is a perennial flower native to North America, including Minnesota. S. lateriflorum is a part-shade to full sun plant that blooms late in the season, generally between late summer and early fall. S. lateriflorum exhibits blooms with a collection of seven or more white petals, forming a panicle inflorescence. The central disk of S. lateriflorum blooms vary in color throughout the duration of the blooming window, ranging from yellow, to purple, to brown (Error! Reference source not found.).

Coreopsis lanceolata (lanceleaf coreopsis) is believed to have potential value in flowering lawns due to the low height of its vegetation, and the ability of C. lanceolata to withstand mowing (Lane, unpublished data). Furthermore, C. lanceolata has been listed as a host-plant for many bee species native to the Midwest region of the United States

(Grundel et al. 2011). C. lanceolata is a perennial flower native to North America, including Minnesota that blooms at about one foot, featuring open blooms with yellow

18 petals that are attractive to a diversity of native bees (Error! Reference source not found.). This flower generally blooms between June and July, preferring full sun or light shade, and dry to moist soils.

The value of T. repens and potential for floral enhancement in turf lawns

As awareness for the health and population status of all bees grows, and urban conservation efforts become more prominent, the turf lawn is an intriguing context to explore further pollinator conservation efforts. For my thesis, I had two main objectives.

First, I aimed to quantify the diversity of pollinators that use a model forb, T. repens, as a source of forage within the public parks of Minneapolis, MInnesota. T. repens was selected based on its prevalence in Minneapolis public parks and previous literature citing it as a species frequently visited by bee foragers. Information about pollinator visitors on this species can elucidate the conservation value of T. repens to urban bees, potentially impacting land management decisions within urban greenspaces. Additionally, I compared visitation by A. mellifera and wild bee species as T. repens density increased.

Hung et al. (2019) presented evidence to suggest that A. mellifera may dominate dense floral patches of a single species. In this study, I hypothesized that A. mellifera abundance would increase more rapidly than wild bee abundance with increasing densities of T. repens.

The second objective of my thesis was to quantify the bee communities that forage on lawns florally enhanced with a mixture of low-growing flowers. To evaluate the effectiveness of this floral seed mix, I compared the diversity of bees on lawns with only

19 naturally occurring stands of T. repens to the diversity of bees on lawns that were florally enhanced with the seed mix. The seed mix included T. repens, Prunella vulgaris ssp.

Lanceolate (Self-heal), and Thymus serpyllum (creeping thyme). I hypothesized that lawns that were florally enhanced with this seed mix would have greater diversity than lawns that contained only naturally occurring stands of T. repens. In addition to supporting more diverse bee communities, I also hypothesized that florally enhanced lawns would support different bee communities than lawns that contained only naturally occurring stands of T. repens.

Chapter 2: Floral Enhancement of Turfgrass Lawns for the Benefit of Bee Pollinators in Minneapolis, Minnesota

Introduction

Human land-use changes that result in the loss or degradation of natural habitat are a leading contributor to the declines of both wild bee populations and A. mellifera health (Winfree et al. 2009; Potts et al. 2010; Otto et al. 2016). Urbanization, the conversion of lands for urban needs, is one of the leading forms of land conversion in the

United States. As of 2005, nearly 80% of the United States population lived in or near urban areas, with developed land accounting for over 100 million acres (McKinney 2005;

USDA 2012). Urban lands are becoming more prominent: an average of 1.5 million acres of natural land, like forests and pastures, were developed annually between 2002 and 2007 (USDA 2012).

As urban areas become more prominent, it becomes increasingly important to consider pollinator conservation within these areas. Urban bees are important pollinators of gardens, parks, urban cultivated lands, remnants of natural areas, and various other green spaces (Frankie et al. 2005; McFrederick and LeBuhn 2006; Fetridge et al. 2008;

Matteson et al. 2008; Tonietto et al. 2011; Larson et al. 2014). To support bees in urban landscapes, there must be available sources of forage for pollen and nectar, as well as suitable nesting sites (Westrich 1996; Wojcik and McBride 2012). Efforts have been made to redesign aspects of urban development to create habitat and forage for pollinators. Green roofs (Brenneisen 2006; Kratschmer et al. 2018), roofs covered with vegetation, have been shown to support diverse bee communities around the world,

21 including 79 bee species observed on green roofs throughout Canada. The potential of urban greenspaces (Gardiner et al. 2013; Sivakoff et al. 2018) to provide habitat for bees and other insects was shown in Cleveland, Ohio where vacant lots were found to support

98 bee species.

Turfgrass lawns account for over 50,000 square miles in the United States and are often the largest green space in developed areas (Milesi et al. 2005). Turf lawns are generally managed through applications of fertilizer, irrigation, and mowing to promote the aesthetics and health of the grass species within them (Turgeon 2008). Between 1997 and 2002, the management costs of turf lawns by professional landscape services to a subset of 25 million homeowners was $28.9 billion (Des Rosiers et al. 2007). The premium placed on lawn management has led to concerns about the sustainability of the landscape. Poorly managed and high-input lawns can be associated with environmental issues including water consumption, pollution, pesticide application and exposure, and fossil fuel use (McPherson et al. 1989; Davis and Truett 2004). Furthermore, lawns under traditional management protocols in urban areas lack habitat for wildlife, including pollinators (Stier et al. 2013).

Well-maintained turfgrass areas can provide a diversity of ecosystem and cultural benefits, including runoff control, carbon sequestration, enhanced human mental health, and reduction of noise pollution, among other benefits (Krenitsky et al. 1998; Qian and

Follett 2002; Stier et al. 2013; Beard and Green 1994). Current efforts in turfgrass science seek to enhance the environmental footprint of the turf lawn. Research on turfgrass species selection has indicated that low-input grass species, specifically the fine

22 fescue grasses (Festuca spp.), can perform well in a lawn setting when irrigation, fertilizer, and mowing inputs are greatly reduced (Dernoeden et al. 1994; Watkins et al.

2011).

While great strides have been made to improve the sustainability of turf lawns by reducing inputs, managing lawns to intentionally benefit pollinators is a more novel concept. Flowering plants within the lawn are traditionally viewed as a nuisance, with consumers spending $450 million on lawn herbicides and plant growth regulators in 2012

(Atwood and Paisley-Jones 2017). Despite the perception by some that lawn flowers are weedy or unsightly, some flower species are able to improve the health and sustainability of a lawn. Lawn legumes like T. repens can mitigate the need to apply fertilizer, as legumes are able to fix atmospheric nitrogen for uptake by plants (McCurdy et al. 2013;

Sincik and Acikgoz 2007).

Allowing naturally-occurring lawn flowers like T. repens to bloom within turfgrass lawns has been proposed as a way of increasing habitat forage in urban areas, while improving the sustainability of the lawn. Studies have found that pre-seeding mechanical disruption strategies and timing of planting can promote the establishment of T. repens, and other low growing floral species in both warm-season and cool-season turfgrasses

(McCurdy et al. 2013; Sparks et al. 2015; Lane et al. 2016). A study detailing forage use by bees in 63 neighborhoods in Chicago, Illinois found that T. repens was the most common plant visited by pollinators (Lowenstein et al. 2019). A similar study found that

T. repens was the most common forb utilized by two pollen generalist bee species

23 throughout Canada, accounting for nearly 7% of all pollen collected off of bee specimens from this survey (MacIvor et al. 2014).

Increasing the diversity of floral resources available to bees within lawns may provide forage for more diverse bee communities. In Lexington, Kentucky, 37 bee species were found on naturally-occurring populations of T. repens and Taraxacum officinale (common dandelion) in park lawns (Larson et al. 2014), including 16 bee species that were unique to T. offinicale. A study conducted in Springfield,

Massachusetts (Lerman and Milam 2016) observed 111 bee species on a wider range of flora within suburban lawns.

Interest in using lawn flowers as a source of forage for pollinators has led to research on how to manage lands to support the co-establishment of flowers and turfgrass species. Reducing the frequency of mowing within a lawn area can increase the numbers of flowers present in the area, providing substantial forage to nearby bee communities

(Shwartz et al. 2013; Lerman at el. 2018). Turfgrass species selection can also affect the ability of flowers to establish within a lawn, as turf species with a slower rate of growth were found to support a greater abundance of flora (Lane et al. 2019a).

Public perception of flowering lawns to support pollinators may be changing. A survey of lawn preferences in April, 2010 suggested that Minnesota homeowners preferred lawns that were free of weed infestation (Hugie et al. 2012). A more recent survey of park visitors in Minneapolis, Minnesota revealed that 95.4% of respondents supported the planting of flowering bee lawns within community parks; consumers felt these lawns were aesthetically pleasing and beneficial to bees (Ramer et al. 2019).

Human perceptions of lawns are often dictated by cultural and neighborhood norms for landscape appearance, as lawns that strongly differ from what is commonplace are not well received by the public. Consumer rankings of lawns found that individuals who had been shown examples of conventional lawns rate the conventional lawn aesthetic the highest, while consumers who had been shown ecologically beneficial lawns prefer the more innovative alternative (Nassauer et al. 2009).

Given a growing body of literature suggesting that lawn flowers may support diverse communities of pollinators, and emerging support for lawn alternatives by the public, it is essential to provide novel ways to support pollinators within turf lawns.

While studies have demonstrated the value that naturally-occurring flowers may hold for pollinators (Larson et al. 2014; Lerman and Milam 2016) and have suggested strategies to enhance the number of flowers observed in a turf lawn, none have implemented a seed- mix designed specifically to provide forage for pollinators. In this study, we aimed to compare bee communities on florally enhanced lawns to bee communities on naturally- occurring populations of Trifolium repens (Dutch white clover). We hypothesized that florally enhanced lawns will support more diverse communities of bees compared to clover-only lawns. We also predicted that the bee community composition on T. repens would differ from the communities observed on the additional floral species that successfully established in the seed mix (P. vulgaris and T. serpyllum). By quantifying the bee communities that forage in florally enhanced turfgrass lawns, we can demonstrate the ecological value of a land management strategy that is easy and effective to implement.

General Methods

Study area

This study took place across 16 public parks (Table 1) in Minneapolis, Minnesota

(Figure 1) between Spring of 2016 and Summer of 2018. The Minneapolis Parks and

Recreation Board provided a list of parks from which to choose for bee sampling, ranging in size from 0.5 hectares to 26.7 hectares and that contained pre-existing stands of T. repens within Poa pratensis (Kentucky bluegrass) or Festuca spp. (fine fescue) turf lawns. Each park was maintained by mowing from at least four inches down to two inches every 10-14 days from early summer through the fall of each year, and no irrigation was applied to any of the locations. Soil samples were collected during the

2016 field season by probing soil from six different locations within the research plot area at each park to a depth of at least six inches. Samples were placed in sterile brown paper bags, to create a homogenous sample for each park, and the University of

Minnesota Soil Testing Lab analyzed each sample for nitrogen, phosphorus, potassium, organic matter, and soil pH.

Floral enhancements

In the fall of 2016, areas within four of the parks were dormant seeded with select floral species to create florally enhanced plots. The parks were selected by dividing

Minneapolis into four quadrants; Northwest, Northeast, Southeast, and Southwest.

Minneapolis interstate 35W served as the boundary between East and West, while

26 interstate 94 served as the boundary between North and South. The areas within the parks to be enhanced were selected in collaboration with administrators from the Minneapolis

Parks and Recreation Board (MPRB). Sites with medium-low shade, limited foot traffic, low weed prevalence, and high public visibility were preferred.

Floral selection

Five floral species were selected for floral enhancement at each of the four selected parks (Figure 2): Trifolium repens, Prunella vulgaris ssp. lanceolata (self-heal),

Thymus serpyllum (creeping thyme), Symphiotrichum lateriflorum (calico aster), and

Coreopsis lanceolata based on previous trials (Lane et al. 2016). The seed mix contained three species native (P. vulgaris, S. lateriflorum, C. lanceolate) to the U.S. as well as two non-native species (T. repens, T. serpyllum). T. repens was seeded at each park to ensure populations of this species did not decrease during subsequent sampling years.

In the fall of 2016, 800 m2 (40 m x 20 m) plots within four parks were florally enhanced by seeding the floral mixture into existing T. repens, following a dormant seeding protocol to ensure that flowering plants had the best chance of germinating the following spring. The turf lawns consisted of either Poa pratensis (Kentucky bluegrass) or Festuca spp. (fine fescue), that had been mowed to a height of 2.54 cm and aerated prior to planting.

Site preparation

In fall of 2016, two forms of pre-seeding disruption, scalping and aeration were applied to the lawn following recommendations from Lane (2016). Directly after pre- seeding disruption, all plants were seeded at the rate of 241 m-2 based on previous trials from Lane (2016). All flower species were mixed together to create a homogenous mixture of bee lawn seeds, which was then mixed with Sustane 4-4-4 starter fertilizer to assist in root establishment following recommendations on the fertilizer bag. The mixture was seeded using a drop spreader, calibrated with walking speed to ensure that flower seed and fertilizer was spread evenly throughout the plot area at each park.

Out of the five bee lawn flowers dormant seeded, the only flowers to successfully bloom in the spring of 2017 were T. repens and P. vulgaris. T. repens bloomed at each of the four enhanced parks as it was already established before seeding. P. vulgaris bloomed at only Kenwood Park and Audubon in spring of 2017. To ensure blooms were observed for each species, plug plants of T. serpyllum, P. vulgaris, S. lateriflorum, and C. lanceolata were installed in early summer 2017 at each of the four enhanced parks.

Thirty-two plugs of each species were installed at each site, for a total of 128 plug plants per site per park. Plug plants were distributed evenly across the 800 m2 surface, with 16 rows of 8 plants each. Plant species alternated by row, with a 2.5m border between each plant. Plugs were watered 2-3 times each week for the first 30 days after planting to ensure successful establishment In the early spring of 2018, an additional 55 plugs of P. vulgaris were planted at each site.

Vegetation surveys

In parks containing only T. repens following each bee survey, vegetation surveys were performed to assess the density of T. repens blooms at each park along the same 30 m transect. A 1 m2 quadrat was dropped once every five meters on each side of the transect from the 0 m marker through the 25 m marker, for a total of 12 measurements per vegetation survey. To obtain an estimate of total T. repens abundance, the observed number of T. repens blooms (flower heads) was multiplied by 5, as only one-fifth of the total area of the transect was sampled. In 2016 and 2017, the abundance of T. repens was counted, and the presence or absence of additional non-target flora (Table 2) was recorded, but their abundance was not quantified. In 2018, in addition to recording the abundance of all flora present within the quadrat, the percentages of turfgrass and bee forage coverage were recorded by visually estimating turfgrass coverage and bee forage coverage within the quadrant each time the quadrant was dropped, and then calculating a grand average for the entire 30 m transect. Bee forage was defined as blooming flowers for these observations. All flora present were identified to species when possible.

At florally enhanced parks, the abundance of each floral species was counted following 30 m fixed transect walks. When conducting meandering transect walks, the total number of enhancement flora present in the 800 m2 area were recorded.

Bee surveys on T. repens

In 2016 through 2018, the abundance and diversity of bees were sampled foraging on T. repens in 16 parks. In 2017 and 2018, bee diversity and community composition were compared at florally enhanced and clover-only parks.

For bees foraging in parks with T. repens only, 264 bee surveys were conducted beginning May 26 at the earliest, and ending September 7 at the latest each year.

Sampling was restricted to the middle of parks where T. repens flowered in coexistence with turfgrass. Bees were sampled along a 30 m fixed transect through these areas for 20 minutes on each survey date between 10 am and 3 pm on days without precipitation, severe winds or heavy cloud cover, and when daytime high temperatures were over 60°F.

Transect locations within a park varied in response to T. repens density and were not always the same for each survey. Bees were collected continuously over the 20 minutes using a Bioquip ® 18-volt, cordless insect vacuum (SKIL 2810). All bees observed actively foraging on T. repens within 1 m on either side of the transect line were collected, stored in collection tubes and placed on ice before they were taken back to the

University of Minnesota Bee Research Facility for identification, curation, and databasing. The time of day, temperature, cloud cover, and wind speed were recorded for each sampling event. This active sampling method was chosen, despite its bias towards larger, or slower bees (Grundel et al. 2011) because passive bowl traps that collect smaller and faster bees could not be utilized due to public access to these traps and sampling restrictions associated with the presence of the federally listed Bombus affinis in

Hennepin county.

Bee surveys on clover-only vs. florally enhanced plots

In 2017 and 2018, the four paired parks (clover-only and florally-enhanced) were visited once per week starting in May, until late August or early September, depending on when blooms were no longer present. Each park was sampled once per week for a total of at least 10 sampling events per site in 2017, and at least eight sampling events in 2018.

Surveys in all parks concluded in August, as flower blooms subsided at this point, with the exception of the florally enhanced park in north Minneapolis in 2018, which was sampled into September due to the presence of late blooming T. serpyllum.

In both years, fixed transect walks were used to sample for bees at paired parks.

At florally enhanced parks sampling was restricted to the 800 m2 where enhancement flowers were seeded. In 2018 while conducting fixed transect surveys, host-plant identifications were recorded for each bee collected. Bees were placed in separate containers for each flowering species present during a sampling event, and when an observer had to alternate containers the timer was stopped for the duration of the transition. Additionally, in 2018, meandering transect surveys were performed once per week at enhanced parks to survey patches of flowers for species that did not bloom in great densities throughout the area that was originally surveyed. A minimum of five meandering transect walks were carried out at each florally enhanced site. Observers walked at a consistent pace for 20 minutes, targeting patches of enhancement flora, when in bloom, with all bees observed collected via bee-vacuum. Bees were stored in separate containers based on the floral species they were collected off of to ensure proper host-

31 plant identifications were recorded. The timer was paused when containers were switched during meandering transect surveys.

Bee identification

Bees were identified to species by Z. Portman using a combination of keys and comparisons to previously identified specimens (Baker 1975; Bouseman and LaBerge

1978; Coelho 2004; Gibbs 2010; Gibbs 2011; Gibbs et al. 2013; LaBerge 1971; LaBerge

1989; LaBerge and Bouseman 1970; Laverty and Harder 1988; Miller et al. 2002;

Mitchell 1960; Mitchell 1962; Roberts 1972; Roberts 1973; Sheffield et al. 2011; Shinn

1967; Williams et al. 2014). A subset of bees (less than 1%) were unable to be identified to species. All specimens were deposited in the University of Minnesota Insect

Collection.

Bees were further classified as either A. mellifera, Bombus, native, or exotic. The native bee classification referred to all native bee species collected, with the exception of those species belonging to the genus Bombus. Bombus was analyzed separately from other native bee species because this group is well-studied, and often used to demonstrate ecological trends observed in native bees. Exotic bees referred to all non-native bee species with the exception of A. mellifera, a non-native species managed by humans

(Larson et al. 2014; Kratschmer et al. 2018; Kennedy et al. 2013).

Bees were subsequently categorized according to their nesting guild and lecticity

(pollen specialization). For nesting guild, bees were described as either “cavity”

(building a large hole or cavity nest made of comb), “ground” (building a hole in a small

32 pile or patch of bare soil), “cleptoparasite” (laying eggs in the nests of other bees), or

“stem/wood” (nest in pithy stems or hollow, woody material left on the ground). One bee species, Megachile rotundata was listed as both a “cavity” nester and as a “stem/wood” nester due to the diversity of nesting substrates it has been observed using (Sheffield et al.

2013; Krombein 1967). Lecticity was split into two classifications: oligolectic (species that exhibit a narrow host-range for pollen collection, collecting pollen primarily within one plant family) or polylectic (species that exhibit a broad host range for pollen collection, visiting plants from different families) (Ritchie et al. 2016). The functional traits of the bee species observed was determined by reviewing a variety of sources detailing their natural history.

Data analysis

Parks with T. repens only

Statistical analyses were performed in RStudio Version 1.1.463 (R Core Team

2018). Species richness was calculated as the total number of unique bee species collected, and was used to estimate the predicted number of species within the community. Species accumulation curves were generated to demonstrate how species richness increased as a function of increased sampling effort (number of sites sampled) using the specaccum function within the package vegan in R (Oksanen et al. 2019). The total number of bee species present within the community was estimated via bootstrapping using the specpool function within the package vegan in R to determine how many bee species utilize T. repens as a source of forage within our study locations.

To determine if there was a relationship between T. repens abundance and bee type, a 33 generalized linear model with a negative binomial distribution was used, using the lme4 package (Bates et al. 2015). In this model, bee abundance served as the response variable, and the explanatory variables for this model were clover abundance, bee type, year, and collection date. Site was included in this model as a random effect. Clover abundance and Julian date were standardized in this model by dividing the raw numbers of each by their standard deviations. This model also included an interaction between bee type and clover abundance to determine if the relationship between bee abundance and clover abundance had different slopes for honey bees and wild bees.

Comparing bee communities at florally enhanced parks and clover-only parks

Statistical analyses were performed R version 3.6.0 (R Core Team 2019). Bee communities at florally enhanced and clover-only sites were summarized at three scales.

First, the diversity of bees found at all paired parks visited between 2016 and 2018 was described by recording the abundance, species richness, nesting guild, and origin (native or exotic) for all specimens.

Second, bee communities were analyzed based on whether bees were collected on florally enhanced or clover-only park plots. The local diversity (a-diversity) of bees at the florally enhanced and clover-only park was measured by calculating the Exponential

Shannon’s index of entropy (Shannon’s entropy) in 2017 and 2018 using the diversity function in the R package diverse (Guevara et al. 2016). Pairs of parks were only included in this analysis if the florally enhanced park had at least one of P. vulgaris or T. serpyllum bloom at some point between 2016 and 2018. In total, five pairs of parks were

34 included in this analysis. A student’s t-test was used to determine if florally enhanced parks had a greater mean bee diversity than clover-only parks.

Finally, changes in bee diversity at florally enhanced and clover-only parks were compared to determine if bee diversity changed more at florally enhanced parks than at clover-only parks. The bee diversity observed during the year before floral enhancement was subtracted from the final bee diversity observed at each park calculated in 2018. The change in bee diversity at enhanced and clover-only parks was then compared using a student’s t-test.

b-diversity was measured to compare bee communities based on enhancement status (florally enhanced or clover-only) and host-flora (T. repens or P. vulgaris + T. serpyllum). Non-metric multidimensional scaling (NMDS) ordination was used to compare the bee communities. The Morisita-horn index was used to provide an abundance-based metric for comparing bee communities, and the Jaccard’s dissimilarity index was used to provide a presence-absence metric for comparing bee communities.

NMDS ordination figures were generated using the ordiplot function in the R package

Vegan. A permanova was then performed using the Adonis function in the R package

Vegan (Oksanen et al. 2019) to determine if there were statistically significant differences between bee communities. Flower visitation was summarized by looking at bee abundance and bee species richness on each floral species.

Results

Floral abundance in Minneapolis public parks

The average abundance of T. repens across all parks was 769 (+/- 47, SE) inflorescences per 1 m 2 quadrat across the 234 vegetation surveys conducted between

2016 and 2018. From this, an average of 3845 total T. repens inflorescences was estimated per 30 m transect. Nine additional naturally-occurring forbs were observed blooming alongside T. repens in turfgrass lawns throughout the sixteen parks sampled.

T. repens bloomed naturally at all paired parks, in all years of data collection, between May 26th and August 23nd. P. vulgaris established at two sites in 2017, and three sites in 2018. T. serpyllum bloomed at one site in 2018. At paired parks, the most abundant floral species was T. repens (µ = 581 +/- 57, SE), followed by P. vulgaris (µ =

117 +/- 32, SE), and T. serpyllum (µ = 10 +/- 4, SE) (Figure 3). C. lanceolata and S. lateriflorum failed to bloom at all sites. In 2018, turfgrass accounted for 54.8% of the land coverage along transects at paired parks, and forb coverage accounted for 5.8% of land coverage. The remaining land coverage (39.4%) within lawns was comprised primarily by weedy vegetation or bare ground.

Bee communities on T. repens

A total of 5038 bees were collected off of T. repens, 5030 of which were identified to species (Table 3). Overall, 56 species from five families and at least 20 genera were collected off of T. repens. Bootstrapping estimated a total visitation of 64 bee species (Figure 4). By group, 2230 individuals (44.2%) were A. mellifera, 765

36 individuals (15.1%) were Bombus, 1148 individuals (22.8%) were native bees not including Bombus, and 895 individuals (17.7%) were exotic bees. Between 2016 and

2018, the number of bee species observed at a site on T. repens ranged from 5 to 17 within a given year. On average (± SD) a single lawn with T. repens hosted 11 bee species (± 3.79) within a year.

Including honey bees, exotic bees represented 62.0% (3125 specimens) of the total bee specimen collected off of T. repens, and 8.9% (5 species) of the species richness observed. The most abundant exotic bee species collected were A. mellifera and Andrena wilkella (59.8% of all specimens observed). The three other exotic bee species observed on T. repens were Megachile rotundata, Anthidium oblongatum, and Hylaeus leptocephalus.

Functional traits of bees on T. repens

In total, 37.65% (1897) of the individual specimens observed were in the ground nesting guild, accounting for 58.92% (33 bee species) of bee species observed on T. repens. Cavity nesters accounted for 61.95% (3121) of the individual specimens observed, accounting for 25.0% (14 bee species) of the bee species observed. Stem/wood nesters accounted for 1.77% (89) of the individual specimens observed, accounting for

8.90% (5 bee species) of bee species observed. Cleptoparasites accounted for 0.16% (8) of the individual specimens observed, and 8.90% (5 bee species) of bee species. Out of the 55 bee species collected off of T. repens, the lecticity was determined for 54 of those

37 species. Polyectic bees represented 48 of the 53 collected bees (88.9%) and 6 of the 54 bee species collected (11.1%) were oligolectic.

Predicting floral visitors on T. repens

Our model suggests that clover abundance (p< 0.001), bee type (p< 0.001), and collection date (p< 0.001) were all significant predictors of bee abundance (Table 4).

Year was not found to be a significant predictor of bee abundance. This model suggests that there is a significant interaction between clover abundance and bee type in predicting bee abundance (p= 0.0134). The model highlighted the following biologically significant patterns: (i) clover abundance showed a positive relationship with bee abundance, (ii)

Julian date showed a positive relationship with bee abundance (Figure 5), and (iii) A. mellifera abundance and wild bee abundance increased at different rates as T. repens abundance increased (Figure 6). A. mellifera abundance and wild bee abundance both had a significant, positive relationship with T. repens abundance: A. mellifera (estimate =

0.705) abundance increased more rapidly than wild bee (estimate = 0.400) abundance with increasing abundances of T. repens (Figure 6; Table 5).

Bee species composition at paired parks

A total of 2780 bees were collected on T. repens, P. vulgaris, and T. serpyllum, at the six paired parks included in the comparison of florally enhanced and clover-only parks (Table 6). Of the 2780 bees collected, 2770 were identified to species. Overall, 53 bee species from 5 families from at least 18 genera were collected. Bootstrapping was

38 used to predict that 61 wild bee species were present at the 6 paired parks (Figure 7).

Five exotic bee species were observed at these parks: Apis mellifera, Andrena wilkella,

Megachile rotundata, Anthidium oblongatum, and Hylaeus leptocephalus. These exotic bees represented 53.6% (1490 specimens) of the total bee specimens collected at paired parks (Table 6). The majority of bee specimens were in the cavity nesting guild; however, the ground nesting guild was the most species rich. The majority of bees observed were polylectic.

Bees collected on Enhanced Vs Clover-only Parks

Between 2017 and 2018, a total of 1826 bee specimens were collected off of T. repens from clover-only parks. Thirty-four wild bee species from 14 genera were observed at clover-only parks. Exotic bees represented 51.8% (945 specimens) of the total bee specimens collected at clover-only parks, despite observing just five non-native bee species foraging at these parks. A. mellifera accounted for 71.3% of the non-native bees observed at clover-only parks between 2017 and 2018.

Four hundred and seventy-seven bee specimens, including 38 species and 15 genera, were collected at florally enhanced parks in 2017 and 2018. Thirteen of these bee species were unique to enhanced parks (Table 6). Apis accounted for 47.1%, of the exotic bees observed at florally enhanced parks.

Florally enhanced parks exhibited greater a-diversity of bees than clover-only parks (Figure 8) (p = 0.046). The mean exponential index of Shannon’s entropy was 8.41 at florally enhanced sites, and 6.98 at clover-only sites. There was a significant

39 difference between the change in bee diversity at florally enhanced parks and the change in bee diversity at clover-only parks (p = 0.038) between 2016 and 2018 (Figure 9). b- diversity of bee communities at enhanced and clover-only parks was numerically but not statistically different when considering species abundance (F=2.89, p= 0.092 Morisita- horn index) (Figure 10); however, they were significantly different from one another based on presence-absence (p=0.006; Jaccard’s dissimilarity index) (Figure 11).

Bees collected by host plant

In 2018, the host plants of the bees were recorded. Two hundred and twenty-three bee specimens were collected while visiting T. repens at enhanced parks in 2018, including 21 wild bee species from 12 genera. Thirteen bee species were unique to T. repens at florally enhanced parks in 2018.

A total of 103 bee specimens were collected off of P. vulgaris and T. serpyllum

(76 and 27, respectively) at florally enhanced parks in 2018 (Table 5), including 20 wild bee species from 7 genera. Seven bee species were collected off of P. vulgaris and T. serpyllum that were not observed on T. repens (Table 6). Exotic bees represented just

2.9% (3 specimens) of the specimens collected off of P. vulgaris and T. serpyllum at enhanced parks in 2018. No honey bees were collected off of either of these two flowers species.

In contrast to the analysis of all bees collected over two years, the analysis of bees collected only on host plants in 2018 revealed no statistically significant differences between bee communities on T. repens and bee communities on P. vulgaris and T.

40 serpyllum according to the abundance metric (F= 9.18, p=0.1; Morisita-horn index)

(Figure 10) nor the presence-absence metric (F=1.38, p=0.2; Jaccard’s dissimilarity index) (Figure 11). The data suggests that host-plant accounted for 69.66% of the variation between bee communities.

Discussion

We found that while lawns in urban parks containing white clover, Trifolium repens, supported a diverse community of bees, enhancing lawns with two additional floral species, Prunella vulgaris and Thymus serpyllum, supported significantly greater bee diversity and community composition, based on Jaccard’s dissimilarity index, compared to clover-only lawns. These results demonstrate the ecological value to pollinators of a relatively easy land management strategy: intentionally enhancing turf lawns with low-growing flowers.

Clover-only parks.

We found 55 species of wild bees (56 species total including A. mellifera) utilized

T. repens as a source of forage over three years, which accounted for greater than 17% of the currently recorded bee species in the state of Minnesota, and was more than twice the number of bee species observed in a study looking at bees on T. repens within urban and suburban lawns of Lexington, Kentucky (Larson et al 2014). As our study was restricted to a narrow geographic range within Minnesota, it is likely that T. repens may provide forage to additional species outside the surveyed areas.

Nearly 93% (51/55) of the non-Apis bee species observed on T. repens within turfgrass lawns were native to the U.S, showing the nutritional value of this floral species to many bees. Native bees were also more abundant than exotic bees, accounting for

1913 of the 2,780 non-Apis species collected. Bombus fervidus, a species of conservation concern (Colla et al. 2012), was collected on T. repens 26 times. B. fervidus was also observed on turf lawns with T. repens in Lexington, Kentucky (Larson et al 2014). A. mellifera was the most abundant species utilizing T. repens, accounting for nearly 45% of visitors, which was similar to Larson et al. (2014) who found A. mellifera accounted for

44.2% of all bee species observed on spring T. repens in Lexington, Kentucky. A. mellifera abundance increased at a greater rate than wild bee abundance with increasing abundance of T. repens blooms, likely due to the ability of honey bees to recruit nestmates to abundant patches of flowers. Honey bee visitation rates have been shown to increase with increasing floral abundance (Essenberg 2014; Hung et al. 2019.

Florally enhanced parks

Florally enhanced lawns had significantly greater bee diversity than clover-only lawns according to transect surveys conducted between 2017 and 2018. Bee diversity was measured using the exponential index of Shannon’s entropy, a metric that incorporates both species abundance and community evenness, without disproportionately favoring either rare or common species (Jost 2006). Lawns that were florally enhanced after the first year of sampling also experienced a greater increase in bee diversity than lawns that contained only T. repens throughout the course of the study.

According to the Jaccard’s dissimilarity index, florally enhanced lawns also supported significantly different bee community composition than clover-only lawns, and marginally different bee communities according to the Morisita-horn index. Species that were abundant in both florally enhanced lawns and clover-only lawns likely reduced differences observed between bee communities according to the Morisita-horn index, an abundance-based metric. Conversely, the Jaccard’s dissimilarity index weights all bees equally regardless of abundance, which placed a greater emphasis on species that were unique to a community, especially those that were low in abundance.

In contrast, when bee communities were compared based on host plant in 2018, the bee community observed on T. repens was not significantly different from bee community observed on P. vulgaris and T. serpyllum by either index. The bees observed on P. vulgaris and T. serpyllum provided a large enough sample size to create statistically significant differences in bee diversity when comparing florally enhanced and clover- only lawns, however the sample size of bees collected off P. vulgaris and T. serpyllum was likely too small to detect differences in bee communities based on host plant records.

We believe that we would have observed differences in bee community composition based on host plant records with a greater sample size of bees collected off of P. vulgaris and T. serpyllum. Also, as 2018 was the first year T. serpyllum bloomed, it is likely that more time was required for this plant to be fully established within lawns.

Despite the low abundance of the enhanced flowers, seven bee species were observed on P. vulgaris or T. serpyllum that were not present on T. repens. Some of these bee species (B. vagans, L. dialictus species 1, L. ephialtum, L. leucocomum L.

43 pilosum, L. weemsi) were singletons and doubletons, and their presence or absence may have been due to chance.

Over 95% of the bees observed foraging on P. vulgaris and T. serpyllum were native species, and A. mellifera was not observed on either P. vulgaris or T. serpyllum.

P. vulgaris flower has a whorled bloom with a deep corolla, such that only very large bees or very small bees may successfully forage on this species. If A. mellifera is unable to forage on P. vulgaris, including this floral species in lawn seed mixes could serve as a source of resource partitioning among bee species. Although bee records on T. serpyllum were limited due to the low abundance of blooms observed, this plant holds great value to bees, in part due to its phenology. T. serpyllum blooms between July and September in

Minnesota, and may serve as a source of forage for bees active late in the season when other plants have stopped blooming.

Floral establishment.

We observed significantly greater bee diversity in florally enhanced lawns as compared to clover-only lawns, even though only two flowers (P. vulgaris and T. serpyllum) established successfully. P. vulgaris established in the first summer after planting at two sites 2017, and in the second summer after planting at one additional site in 2018. Delayed blooming for P. vulgaris is not uncommon (Lane 2019b).

Furthermore, both P. vulgaris and T. serpyllum were abundant in low numbers relative to

T. repens through our surveys. The greater bee diversity at florally enhanced sites relative to clover-only sites demonstrates that even small increases in floral diversity can

44 benefit bee communities. Improved floral establishment of intentionally seeded flowers may offer further benefits to bee communities, as significant relationships have been shown between floral abundance and bee abundance (Banaszak 1996) and floral abundance and bee species composition (Potts et al. 2003).

Taking further measures to improve floral establishment may result in increased success when seeding flowers in a lawn area. Utilizing germination blankets and irrigation after seeding to help plants retain moisture, and reducing competition from weeds and foot traffic during plant establishment, may have increased the abundance of

P. vulgaris and T. serpyllum within the public parks. We were unable to minimize weed pressure through the use of herbicides as herbicide use is restricted within public parks in

Minneapolis, Minnesota. We suspect that flora failed to establish at Matthews Park due to soil compaction and wear damage, as our site was located at the bottom of a popular sledding hill. Two floral species, C. lanceolata and S. lateriflorum failed to establish at any of the enhanced sites. These flowers were likely outcompeted for resources by the turfgrass. Both C. lanceolata and S. lateriflorum are generally maintained at taller heights and are not often found in lawn settings.

Conclusions.

These results demonstrate how flowering lawns can support diverse communities of bees while still maintaining the recreational function of the conventional turf lawn.

Floral cover accounted for just under 6% of total land cover within flowering lawns, with turfgrass occupying the majority of lawn coverage, which allows homeowners and land

45 managers to maintain the aesthetics and recreational value traditionally associated with lawns while still providing valuable forage to pollinators. Furthermore, flowering lawns are sustainable, utilizing low-input grass and flower species. Clover-only lawns can serve as forage for both wild bee and A. mellifera communities. Homeowners and land managers should allow T. repens to persist in lawns due to its value to bees, in addition to the value nitrogen fixation provides for maintaining the health of a lawn. Land managers who are open to ecologically innovative landscape designs may want to consider utilizing florally enhanced lawns, which supported more diverse bee communities and greater visitation by native bees than clover-only lawns.

Table 1. List of sites where bee specimens were collected off of T. repens blooms within turfgrass lawns of Minneapolis public parks.

Site Quadrant Park Area (ha) Number of Surveys Audubon North East 2.3 28 Bancroft South East 1.8 6 Brackett South West 4.2 3 Farview North 8.5 10 Hall North 2.4 6 Kenwood South West 13.3 25 Linden Hills South West 3.2 4 Logan North East 4.2 11 Longfellow South East 3.3 27 Matthews South East 4 26 North Commons North 10.3 20 Painter South West 1.2 28 Powderhorn South East 26.7 9 Washburn Fair oaks South West 3.1 10 Willard North 0.5 23 Windom North East 3.3 28

Table 2. Species names and associated traits of species selected for floral enhancement of turfgrass parks in Minneapolis, Minnesota.

Table 3. Species list including abundance and functional traits of bee specimen collected

off of T. repens blooms in turfgrass lawns of parks in Minneapolis, Minnesota. Origin

was defined as either native (N) or exotic (E). Foraging refers to pollen collection

behavior.

Family Bee Abundance Nesting Origin Foraging Group Halictidae Agapostemon 59 Ground N Polylectic Wild sericeus Halictidae Agapostemon 8 Ground N Polylectic Wild texanus Halictidae Agapostemon 6 Ground N Polylectic Wild virescens Andrenidae Andrena carlini 1 Ground N Polylectic Wild Andrenidae Andrena 4 Ground N Polylectic Wild commoda Andrenidae Andrena 5 Ground N Polylectic Wild dunningi Andrenidae Andrena 1 Ground N Polylectic Wild imitatrix Andrenidae Andrena vicina 6 Ground N Polylectic Wild Andrenidae Andrena 781 Ground E Oligolectic Exotic wilkella Andrenidae Andrena 25 Ground N Unknown Wild wilmattae Halictidae Anthidium 36 Cavity E Polylectic Exotic oblongatum Apidae Apis mellifera 2230 Cavity E Polylectic Apis Halictidae Augochlorella 36 Ground N Polylectic Wild aurata Apidae Bombus 1 Cavity N Polylectic Bombus auricomus Apidae Bombus 73 Cavity N Polylectic Bombus bimaculatus Apidae Bombus 26 Cavity N Polylectic Bombus fervidus Apidae Bombus 23 Cavity N Polylectic Bombus griseocollis

Apidae Bombus 461 Cavity N Polylectic Bombus impatiens Apidae Bombus 180 Cavity N Polylectic Bombus rufocinctus Apidae Bombus vagans 1 Cavity N Polylectic Bombus Andrenidae Calliopsis 425 Ground N Oligolectic Wild andreniformis Megachilidae Coelioxys 1 Cleptoparasite N Polylectic Wild rufitarsis Colletidae Colletes 2 Ground N Oligolectic Wild kincaidii Colletidae Colletes 1 Ground N Oligolectic Wild robertsonii Halictidae Halictus 230 Ground N Polylectic Wild confusus Halictidae Halictus ligatus 2 Ground N Polylectic Wild Halictidae Halictus 268 Ground N Polylectic Wild rubicundus Megachilidae Heriades 1 Cavity N Polylectic Wild carinata Megachilidae Hoplitis 3 Stem/Hole N Polylectic Wild producta Megachilidae Hoplitis 1 Stem/Hole N Polylectic Wild truncata Colletidae Hylaeus 1 Stem/Hole E Polylectic Exotic leptocephalus Halictidae Lasioglossum 1 Ground N Polylectic Wild admirandum Halictidae Lasioglossum 2 Ground N Polylectic Wild anomalum Halictidae Lasioglossum 1 Ground N Polylectic Wild cinctipes Halictidae Lasioglossum 1 Ground N Polylectic Wild heterognathum Halictidae Lasioglossum 5 Ground N Polylectic Wild hitchensi Halictidae Lasioglossum 1 Ground N Polylectic Wild imitatum Halictidae Lasioglossum 4 Ground N Polylectic Wild lineatulum Halictidae Lasioglossum 11 Ground N Polylectic Wild paradmirandum

Halictidae Lasioglossum 1 Ground N Polylectic Wild platyparium Halictidae Lasioglossum 1 Ground N Polylectic Wild pruinosum Halictidae Lassioglossum 1 Ground N Polylectic Wild tegular group Halictidae Lasioglossum 1 Ground N Polylectic Wild viridatum Halictidae Lasioglossum 2 Ground N Polylectic Wild weemsi Halictidae Lasioglossum 1 Ground N Polylectic Wild zephyrum Megachilidae Megachile 1 Cavity N Oligolectic Wild campanulae Megachilidae Megachile 8 Cavity N Polylectic Wild frigida Megachilidae Megachile 7 Stem/Hole N Polylectic Wild latimanus Megachilidae Megachile 77 Cavity/ E Polylectic Exotic rotundata Stem/ Hole Megachilidae Megachile 1 Ground N Polylectic Wild texana Apidae Melissodes 3 Ground N Oligolectic Wild subillata Apidae Nomada sp.1 2 Cleptoparasite N Polylectic Wild Apidae Nomada sp.2 3 Cleptoparasite N Polylectic Wild Apidae Nomada sp.3 1 Cleptoparasite N Polylectic Wild Megachilidae Osmia pumila 3 Cavity N Polylectic Wild Halictidae Sphecodes sp.1 1 Cleptoparasite N Polylectic Wild

Table 4. Summary of results of generalized linear mixed model with bee abundance as the response variable and bee type (wild or A. mellifera), clover abundance, Julian date, and year as the explanatory variables. An interaction between bee type and clover abundance was included in the model. Site was included as a random effect.

Factor Estimate Z p-value

Intercept -1.81570 -1.882 0.0599

Bee type 0.89 4.905 <0.001*

Clover abundance 0.70513 7.402 <0.001*

Julian date 0.45245 7.975 <0.001*

Year (2016) -0.86793 -1.098 0.2723

Year (2017) -1.12027 -1.407 0.1595

Year (2018) -0.69547 -0.873 0.3828

Bee type x clover abundance -0.30556 -2.474 0.0134*

Table 5. Comparison of slopes for the change in bee abundance with increasing T. repens abundance for A. mellifera and wild bees. LCL represents the lower confidence limit, and UCL represents the upper confidence limit, according to a 95% confidence interval.

Bee type Estimate SE df LCL UCL

A. mellifera 0.705 0.0953 inf 0.518 0.892

Wild bee 0.400 0.0923 inf 0.219 0.581

Table 6. Bee species collected off of flowering lawns at paired parks in Minneapolis,

Minnesota between 2016 and 2018.

Family Species Abundance

Andrenidae Andrena carlini 1

Andrena commoda 2

Andrena dunningi 4

Andrena vicina 1

Andrena wilkella 381

Andrena wilmattae 5

Calliopsis andreniformis 213

Apidae Apis mellifera 1040

Bombus auricomus 1

Bombus bimaculatus 44

Bombus fervidus 20

Bombus griseocollis 10

Bombus impatiens 385

Bombus rufocinctus 110

Bombus ternarius 1

Bombus vagans* 2

Melissodes bimaculatus 1

Melissodes subillata 2

Nomada species 1 1

Colletidae Colletes kincaidii 2

Hylaeus leptocephalus 1

Halictidae Agapostemon sericeus 33

Agapostemon texanus 5

Agapostemon virescens 3

Auguchlorella aurata 71

Dufourea monardae* 4

Halictus confusus 146

Halictus ligatus 1

Halictus rubicundus 142

Lasioglossum admirandum 1

Lasioglossum anomalum 21

Lasioglossum dialictus

species 1+ 3

Lasioglossum ephialtum* 1

Lasioglossum heterognathum 1

Lasioglossum hitchensi 9

Lasioglossum illinoense 1

Lasioglossum leucocomum* 2

Lasioglossum lineatulum 1

Lasioglossum

paradmirandum 10

Lasioglossum pilosum^ 1

Lasioglossum pruinosum 3

Lassioglossum tegular

group 6

Lasioglossum weemsi^ 2

Lasioglossum zephyrum 1

Megachilidae Anthidium oblongatum 22

Coelioxys rufitarsus 2

Hoplitis producta 3

Hoplitis truncata 1

Megachile campanulae 1

Megachile frigida 4

Megachile latimanus 3

Megachule rotundata 46

Megachile texana 1

Osmia pumila 2

Figure 1. ArcGIS-map of Minneapolis, Minnesota and surrounding areas depicting site locations (thumbnails).

Figure 2. Candidates for floral enhancement for turfgrass lawns. Top row (left to right)

Trifolium repens, Prunella vulgaris, Thymus serpyllum. Bottom row (left to right)

Coreopsis lanceolata, Symphiotrichum lateriflorum.

Figure 3. Mean (+/- SE) abundance of lawn inflorescences observed within flowering lawns in Minneapolis, Minnesota in 2018. Flowers were counted along a thirty meter, fixed transect, immediately following bee surveys along the same transect line. Dates above each bar indicate the bloom period for each species in 2018.

Figure 4. Species accumulation curve for bees collected off of T. repens at Minneapolis public parks. A total of 56 bee species were collected, and bootstrapping suggests that 64 bee species may be present within this community.

Figure 5. Bee abundance on T. repens blooms within Minneapolis parks throughout the growing season, sorted by Julian date.

Figure 6. Linear regression depicting the relationship between bee abundance and T. repens abundance in turfgrass lawns of 16 public parks in Minneapolis, Minnesota. The black line represents the relationship for A. mellifera, and the gray line represents the relationship for wild bees. The shaded area around each line depicts confidence intervals.

Figure 7. Species accumulation curve for bees collected at paired parks in Minneapolis.

A total of 53 bee species were collected, and bootstrapping suggests that 61 bee species may be present within this community.

Figure 8. Exponential Shannon's index of entropy at clover-only and florally enhanced parks in Minneapolis, Minnesota, 2016-2018. Florally enhanced parks exhibited greater diversity (p= 0.046) than clover-only parks.

Figure 9. Change in the Exponential Shannon's index of entropy at enhanced and clover- only parks between 2016 and 2018. Parks that were florally enhanced exhibited a greater increase in diversity (p=0.038) than parks that remained clover-only during this time frame.

Figure 10. Non-metric multidimensional scaling ordination of the community composition of bees collected at florally enhanced and clover-only park in Minneapolis,

Minnesota, 2017-2018, according to the Morisita-horn index.

Figure 11. Non-metric multidimensional scaling ordination of the community composition of bees collected from enhanced and clover-only parks in Minneapolis

Minnesota, 2017-2018, according to the Jaccard dissimilarity index.

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A1. Naturally-occurring weedy species observed within flowering lawns. Bees were not collected off of these species as they were not observed in high abundance on these flowers.

Appendix A

A2. Non-metric multidimensional scaling ordination of the community composition of bees collected off of T. repens and P. vulgaris + T. serpyllum at Minneapolis parks in

2018, according to the Morisita-Horn index.

A3. Non-metric multidimensional scaling ordination of the community composition of bees collected off of T. repens and P. vulgaris + T. serpyllum according to the Jaccard dissimilarity index.