Urban ornamental plants for sustenance of wild bees (Hymenoptera, Apoidea)

The aim of our study was to assess the attraction and value of flowering plants at green areas in support and sustenance of wild bees (Hymenoptera, Apoidea) populations in Kyiv. Study objects were the most common flowering ornamental plants of the city and the wild bees visiting their inflorescence during the vegetation season to collect pollen and feed on nectar. The study was conducted at 16 areas of observation and material collection, which include urban parks, M.M. Gryshko National Botanical Garden, green spaces of residential areas, roadsides, etc. Insects were collected following the standard method of catching individual specimens during the spring and summer periods of 2012–2018. Based on the observations, we visualized trophic relations of bees with plants and calculated the biodiversity index of visiting insects for plants. The blossom periods were analyzed using phenological data. Examination of urban green areas revealed ornamental plants that were the most attractive for bees, including more than 35 taxa of 20 families of trees, shrubs, and grassy plants. Bees are superiorly attracted to plants of the genera Rudbeckia, Sedum, Gypsophila, Cerasus, Tagetes, Spiraea, Lonicera, and Aesculus. There is a succession of plant flowering during spring-summer season, which must be considered while planting of greenery. Certain plant species attract insects at each blossom period, for example, Prunus, Rhododendron, Crataegus, Aesculus in spring, most of Asteraceae – in summer. The diversity of blossoming plants is significantly lower at the end of summer and beginning of fall, coinciding with the decreasing flight activity of wild bees. Overall, the studied ornamental plants attract not only the most common species of wild bees but also highly specific and rare species such as Bombus argillaceus and Xylocopa valga, protected by the Red Data Book of Ukraine. We found that blossoming green areas made up of trees, shrubs, and herbs are essential for feeding many species of wild bees and sustaining their populations in urban conditions.


Introduction
The urban environment becomes increasingly important to the sustenance of biodiversity, which is critically endangered by the combined effects of intensive agriculture, agrotechnical measures, and use of pesticides (Chiesura, 2004;Winfree et al., 2009;Dearborn & Kark, 2010;Sanderson & Huron, 2011). The humankind is now facing the problem of extinction and rapid decline of pollinator populations (Potts et al., 2010), including the wild bees (Hymenoptera, Apoidea). Those insects are considered the best pollinators because they pollinate almost 80% of flowering plants (Klein et al., 2007;Smitley, 2018).
Botanical gardens, parks, and garden squares are especially significant for the preservation of biodiversity (Hammitt, 2002; G.Y. Honchar, A.M. Gnatiuk Mexia et al., 2018). For many plants, there are conditions to grow ex situ in botanical gardens and parks. The general composition of green areas of Kyiv, their protective and purifying functions, esthetic value and conservation significance were described in numerous publications (Cherevchenko et al., 1999;Cherevchenko & Kuznetsov, 2003;Rubtsova, 2006;Doyko, 2012;Klymenko, 2012;Hatalska & Kryvenko, 2012;Rogovskiy, 2013;Pikhalo, 2014;Melezhyk, 2015;Matiashuk et al., 2015). Trees and shrubs are essential food sources for bees (Somme et al., 2016). The species composition of trees of urban plantations in Kyiv includes a lot of plants that are attractive to bees: 39.6 % linden, 22.2 % horse chestnut, 4.0 % Norway maple, and nearly 2 % black locust and rowan (Lesnik, 2015). However, their distribution is limited, and flowering is rather short-term. As for shrubs, only 20 of recorded species are decorative bloomers, representing only 6.7 % of all shrub species in collections of the botanical gardens of Kyiv (Oleksiychenko & Breus, 2013).
The primary factors limiting the sustenance and persistence of wild bee populations are feeding and nesting resources. Places for bees to nest are more or less present in urban biotopes. Species that nest in the soil can use fragments of soil cover at roadsides, garden squares, urban parks; those that use plant material can nest in deadwood in parks and private plots; for those preferring hollows, there are walls of buildings and fences. However, the foraging resources (flowers) are often limited due to the impoverished composition of plants. This fact also negatively impacts the growth and reproduction of bee populations.
Overall, the trophic relations of wild bees have been studied extensively in cities of other countries. Many authors have pointed out the significance of decorative green areas (with blossoming trees, shrubs, and herbs) as foraging resources for bees (Gathmann & Tscharntke, 2002;Acar et al., 2007;Hennig & Ghazoul, 2011;Garbuzov & Ratnieks, 2014;Hausmann et al., 2016;Garbuzov et al., 2017;Lowenstein et al., 2019;Sikora, 2019;Erickson et al., 2020). However, the attractiveness and value of decorative green areas with various plant species to wild bees have not been studied in urban conditions before.
Our work aimed to study the trophic relations of wild bees with flowering plants of the green areas of Kyiv.

Material and methods
Studies were conducted in Kyiv during the spring and summer seasons of 2012-2018. Model areas were located in the M.M. Gryshko National Botanical Garden of NAS of Ukraine (a significant hotbed of phytodiversity), and urban parks "Feofaniya", "Nyvky", "Peremoha", "Partizans'koi slavy". Also, the ornamental green plantations of residential areas "Teremky 1", "Vynohradar", as well as the avenues, roadsides, stops of civil transport, and road intersections were studied (Fig. 1).
Here, we consider the most common flowering ornamental plants (more than 35 taxa) of green areas and decorative plant compositions of the model territories, in relation to their attractiveness to bees. Bees were collected with an insect net while bees were visiting flowers (Pesenko, 1982). The visited plants and their botanical family membership were recorded. Individual specimens were caught, euthanized with ethyl acetate, and brought to the laboratory for species identification. We chose the most common bee species found in a city from our previously published check-lists of wild bee species (Honchar, 2017;Honchar & Gnatiuk, 2018;Radchenko & Honchar, 2019) to determine their trophic relations. In total, around 50 species of wild bees are considered here from the families Сolletidae ( Urban ornamental plants for sustenance of wild bees (Hymenoptera, Apoidea) The trophic relations were visualized in R version 3.6.1 (R Core Team, 2014) using the "bipartite" package (Dormann, 2011(Dormann, , 2020. Trophic relations between bees and the respective plants are presented graphically. The width of relation on one side indicates the number of visits and diversity of visitors for plants, and on the other side for bees (Figs. 2 & 3).
We used the diversity index S for the bee visitors of flowers ( Table 1). The index is based on Fisher's α (Fisher et al., 1943;Magurran, 2013;Dormann, 2020).

Results
The bee species differed by periods of their flight activity and nesting specifics. Some of them build their nests in soil, other -in plant material, for example, members of the family Megachilidae or the genus Hylaeus prefer hollows. There were solitary bees, inquilines (Sphecodes spp.), and eusocial species (Bombus). The main trophic relations that we have observed in the system "beeangiosperm" are represented on Figs. 2 & 3.
The bipartite network ( Fig. 2 & 3) constitutes weighted representations of the plant-pollinator interactions. We used the frequency of flower visits by bees as the interaction weight to construct the network. The number of relations and index of diversity for each plant are given in Table 1.

G.Y. Honchar, A.M. Gnatiuk
As can be seen from Table 1 and Figs. 2 & 3, there are plant species that attract more than 10 wild bee species. However, there are plants such as Spirea, which mostly attract the most common bumblebee species and abundant species of the genus Evylaeus, less so other wild bees. Similarly, flowers of Gypsophila paniculata, Dahlia, and Tagetes attract a significant number of these insect species. However, the visitor diversity index is 3 to 6 in these cases because of the domination of certain species. Some plant species, such as Calendula, Coreopsis, Rudbeckia, Sedum L., Prunus, attract pollinators more evenly. In general, the bee species with higher ecological plasticity dominate in the urban environment, though specific oligolectic pollinators of certain species also are represented (Banaszak-Cibicka & Żmihorski, 2012; da Rocha-Filho, 2018). Those bees are attracted to plants of the genus Malva (specifically, Tetralonia malvae (Rossi, 1790), bees eat pollen from these flowers), Campanula (to which Andrena curvungula Thomson, 1870 is specialized), Stachys and Digiatalis are pollinated by Anthidium manicatum (Linnaeus, 1758) and Osmia bicolor (Schrank, 1781).
Aesculus hippocastanum L. attracts eight of the most common wild bee species, including two protected by the Red Data Book of Ukraine (Radchenko, 2009;Radchenko et al., 2009), Bombus argillaceus (Scopoli, 1763) and Xylocopa valga Gerstaecker, 1872. Bees of the latter species have a lot of various trophic relations on the studied territory. Fruiting trees of the family Rosaceae that are planted in green areas are also essential for bees in early spring throughout the season, especially in herb-free urban biotopes.
We have found that bees are more attracted to plants from the following 20 families. Families Asteraceae and Rosaceae were exceptionally diverse by the number of plant taxa visited by bees (Table 1; Fig. 4). At the same time, several families which were presented by only one or two genera (such as Tamaricaceae and Sapindaceae) are significant for feeding of wild bees of various species.  There are seasonal fluctuations in the species diversity of wild bees. Overall, wild bees begin their flight activity in the middle of March though that is notably dependent on weather conditions. The highest level of bee diversity is observed in May and June, then again in early July, and declines in August. During the large-scale distribution and reproduction of bees, the presence of pollen and nectar reserves is critical, affecting the nutritive qualities of feeding resources, and most importantly, the collection of a provision intended for broods. Thus, a continuance of blossom is needed from March to September. According to our data, it is not found in a number of parks, and less so at roadsides, in flowerbeds and garden squares. Therefore, the assortment of angiosperms does not provide the succession of flowering plants to sustain wild bees. Some plant species bloom only in early spring, others only in summer. Only by combining plants with varying periods of flowering, it is possible to sustain wild bees with good-quality nutrition resources. In Kyiv, the most common and attractive for bees ornamental plants flower from the end of April till the middle of August (Fig. 5). This fact indicates the incompleteness  Urban ornamental plants for sustenance of wild bees (Hymenoptera, Apoidea) of feeding resources for bees in early spring and autumn.

Discussion
Urban ornamental plants are usually introduced species. The nectar they produce may contain metabolites, which are unattractive, unusable, and even poisonous to bees due to the narrow ranges of feeding preferences of the latter (Novotny & Basset, 2005;Dyer et al., 2007). An example of such a plant is Tilia tomentosa Moench, with nectar that can cause mass mortality of bumblebees (Koch et al., 2017;Jacquemart et al., 2018).
We would like to note that this plant is rarely used in green areas of Kyiv, only sometimes in residential areas and collections of botanical gardens and arboretums. Double-flowered plants are widely used for ornamentation of green areas and present another problem for the foraging bees. Such plants are less attractive for pollinators due to lower production of nectar and accessibility of flowers (Comba et al., 1999;Corbet et al., 2001). According to our data, double-flowered cultivars of the genera Dahlia, Tagetes, Рaeonia L., and Rosa were indeed less attractive for bees compared to the cultivars with simple flowers. Among other ornamental and widely used plants, cultivars of Petunia Juss. had low value for bees. Their flowers produce nectar and pollen in low quantities, and their deep and narrow corollas limit the access to the flower in general. Varieties and cultivars of Ageratum L., Hydrangea L., Viola × wittrockiana, and Begonia L. are also unattractive for bees.
On the other hand, there are such widely grown, aggressive introduced species as Robinia pseudoacacia L., Amorpha fruticosa L., Solidago canadensis L., S. gigantea Aiton and Asclepias syriaca L. They are considered to be quality honey plants, rich with nectar and pollen, with long periods of flowering and at times presenting the only foraging resource for bees. However, their ability to displace other plants has negative effect on the ecosystem as a whole (Salisbury et al., 2015;Baker & Potter, 2018;Jachuła et al., 2020). Therefore, using species of the natural flora of Ukraine to maintain green areas is preferable, because that would also sustain the populations of rare and specialized species of wild bees (Gnatiuk & Gaponenko, 2018). We think that using species of the genera Tamarix and Rhododendron (in particular, R. dauricum) would be advantageous in the maintenance of urban green areas because these plants are of high ornamental value and produce nectar and pollen for many wild bee

Conclusions
Parks, botanical gardens, garden squares, and other green areas sustain the biological diversity in cities. For pollinators, whose populations face a worldwide decline, the flowering plants of green areas are especially important. We examined more than 35 species of plants of 20 families and observed the highest bee diversity on plants of the families Asteraceae, Rosaceae, and Lamiaceae. The most attractive plant species under study belong to the genera Aesculus, Rhododendron, Rudbeckia, Sedum, Gypsophila, Prunus, Malus, Tagetes, Spiraea, Lonicera, and Tamarix. Certain plant species, for example, from the genera Malva, Campanula, Stachys, and Urban ornamental plants for sustenance of wild bees (Hymenoptera, Apoidea) Digitalis attract specialized bee species. Ornamental angiosperms also provide pollen and nectar to species listed in the Red Data Book of Ukraine, Bombus argillaceus and Xylocopa valga.
In our opinion, the plants used in urban green areas should not have decorative value only but also provide pollen and nectar to the wild bees of urban landscapes. To ensure the excellent nutritive resources for bees, the assortment of flowering plants should be continuous, and cultivars and varieties with simple flowers should be a preference for the green areas. Of particular interest are earlyflowering species and plants which bloom in autumn. Using plant species with lowproductive flowers which are inaccessible for insects should be limited. Introduced plants, which are tolerant of urban conditions and actively produce seeds and self-propagate, should be avoided.
It should be noted that the assortment of ornamental plants used in urban green areas is continuously growing. Thus the studies of trophic relations between the wild bees (and insects in general) have to be continued. That would provide scientific recommendations for the selection of species and cultivars of esthetically pleasing plants that ensure the survival of many groups of insects in urban conditions. Druzhby Narodiv blvd.