Ornamental Bee Plants as Foraging Resources for Urban Bees in Southern Brazil

Ornamental plants are distinguished by the shape and color of their leaves/flowers and their use in landscaping and gardening. In urban areas, their presence is relevant for the maintenance of bees. Aiming to list the ornamental bee plants species occurring in Santa Catarina State (SC), southern Brazil, a survey of forage resources for bees, recorded in the State, was performed. We refer all published works developed in SC (resulting in the period 1983-2014) which include data from reports of scientific research, monographs, dissertations, Masters Dissertations, Doctoral Thesis, annals of scientific events, scientific articles and books. From the 28 ensuant works, we listed, as ornamental bee plants occurring in SC, 201 species, of 156 genera and 66 botanical families. Of these species, 92 are native (N), 26 endemic to Brazil and 109 exotic (E). Families with more ornamental bee species are: Fabaceae (22 species), Asteraceae (20), Solanaceae (11), Rosaceae (10) and Lamiaceae (8). The most cited species are: Lantana camara L. (N) (Verbenaceae) (9 quotes), Aloysia virgata (N) (Ruiz & Pav.) Juss. (Verbenaceae) (8), Hedychium coronarium J. Koenig (naturalized) (Zingiberaceae) (6) and Brachyscome multifida (E) (Asteraceae) (5), regarding habitus, herbs (48.5%) predominate, followed by bushes (21.5%), trees (16.5%) and vines (10.5%). Preferred colours of flowers by bees are, in decreasing order: white, yellow, red/pink, and others. The genus Ipomoea, Calliandra, Passiflora, Prunus and Senecio have more ornamental bee plant species. A large botanical diversity arises, demonstrating the possibilities for urban bee foraging and ornamental featuring, in a perspective of sustainability.


Introduction
Crops depend on pollination to have viable economic returns.Apis mellifera is the most widespread pollinator in the world, however, this species is nowadays affected by CCD (Colony Collapse Disorder) [1].It has been hypothesized that pollination will depend increasingly on native bees for the transfer of plant gametes [2].Native bees live spontaneously in natural areas but also in urban areas [3].Natural areas are shrinking worldwide in view of human interventions in the environment and it has been observed that urban areas have been progressively occupied by populations of non-domesticated species, thus turning into havens for wildlife [4].It is known that crops have higher yields if they are contiguous to areas of native vegetation cover that act as sources of pollinators [5].In urban areas, pollinators exploit existing open areas (gardens, orchards, squares, parks, sports fields, clubs, vacant lots, vacant areas, etc...) where there are flowering plants of ruderal, ornamental, fruit trees, vegetables, weeds and others species, of varying sizes and habits [6].Thus, it becomes relevant, in urban areas, to have bee plants for maintaining the diversity of bees.The goal of offering more floral resources for bees in urban areas can be achieved by encouraging the growing of ornamental bee plants, in a perspective of gardening, landscaping and sustainability [7].Plants known as ornamental are distinguished by the attractive shapes and/or colors of their leaves and/or flowers and are part of numerous groups of cultivated and wild species, including representatives of various botanic families [8].They are often cosmopolitan and originating from different countries [9].
Santa Catarina (SC) is a state in southern Brazil, with 95,400 km 2 of surface (an area equivalent to Austria, Hungary, Ireland or Portugal), subtropical-temperate (including frosts and eventually snow in winter), which shows a strong relief in the form of an increasing altitudinal gradient in an east (Atlantic Ocean)-west (border with Argentina) direction (750 km spacing), with 77% of its territory above 300 m altitude and 33% above 600 m, with a maximum altitude of 1822 m (Morro da Igreja Mountain), vegetation cover with the Atlantic Forest biome (rain forest), strong agricultural production (cereals, temperate fruit orcharding) [10].Although it is the second largest exporter of honey from Brazil (coming from colonies of Apis mellifera), the state has suffered with the CCD [11].
Previous surveys of bee species and works related to bees have been done in SC and included lists of bee plants as their floral resources, forming a mass of information about bee-flower relationships.However, none of them was directed to the observation of foraging of bees on ornamental plants.These works gave rise to the question about whether there are ornamental bee plants cited amidst all the papers and, more specifically, of whether type are these plants in terms of habitus, flower color and geographical origin.The aim was to enroll particular ornamental plants, aesthetically pleasing, suitable for gardening and landscaping, to be used, in urban areas, as a draw and food resource for wild bees.This was thought in a view of making it possible for ecologists, farmers, plant enthusiasts and gardeners, to enhance the urban environment as a biological corridor, connecting nearby forest fragments.

Material and Methods
The work was done during the year of 2014.The analyzed papers compose the library of the LABEL-Bee Laboratory of the University of the Region of Joinville.The period covered by the papers runs from 1983 to 2014.The works include academic data (scientific initiation reports, monographs, Masters dissertations, Doctoral thesis), technical reports, proceedings of scientific events, scientific articles, book chapters and books.We selected 28 works considering the following criteria: the work had been done in Santa Catarina State and the subject was about bees in any of the following themes: bee rearing, surveys of species, pollination studies, palinology of bee plants, bee pollinators or related ones.The procedure for the selection of ornamental bee plants of Santa Catarina State followed the steps described hereafter (Figure 1).After compiling all the works, we searched for the theme bee plants in each paper.All the plants mentioned in each paper were listed in a database.The habitus, color of flower/inflorescence, geographical origin and ornamental condition of the species were looked for and digested.The ornamental plants were then selected from the database to constitute the list of ornamental bee plants occurring in SC State.

Results and Discussion
We listed, from the 28 selected works, 956 bee plant species for SC, from which we verified, as ornamental ones, 201 species, 156 genus and 66 families (Table 1).In urban areas in southern Brazil, [12] reported 64 bee species, [13] 85, [14] 154, [15] 69 and [16] 42.The percentage of ornamentals found in this work constitute 21.02% of the bee plant species mentioned for SC.No information about this percentage for Brazilian studies was in literature.
The family that shows more ornamental bee plant representatives is Fabaceae with 22 species, followed by Asteraceae (20), Solanaceae (11), Rosaceae (10), Lamiaceae (8), Verbenaceae and Bignoniaceae (7), Cactaceae and Malvaceae (6), among others (Figure 2).[14] mention Fabaceae as the the most represented bee plant species as well as [16].[17], [18] and [19] found that the three botanical families with more bee plant species were Asteraceae, Myrtaceae and Fabaceae and [20] mention that the the two most attractive plant families to bees were Asteraceae (which provide pollen and nectar) and Lamiaceae (which provide nectar).Fabaceae is a very large family in tropical and subtropical South American habitats, with 2801 species in Brazil [21] and is very visited by bees, the flowers often shaken to free the pollen out of the porate anthers (buzzing) [22].Asteraceae totals 2064 species in Brazil [23] and shows a floral display of the open type, much sought after by bees because of the ease to land, the conspicuousness of the flowers in the wild and the arrangement of the inflorescences opening in sequence, offering new supplies every day [24].Solanaceae has greatest diversity of species in South America and Central America, with approximately 470 species in Brazil [25] and its flowers also pass by sonication to have its pollen freed by bees [26].The other families are reported as having also species attractive to bees [27].
The genera with more ornamental bee plant species are Ipomoea, Calliandra, Passiflora, Prunus, Senecio and Tibouchina with 4 species each one and Acacia, Aloe, Begonia and Rosa with 3 (Figure 3).The differences in ornamental plant presence and abundance are important variables (suggesting different gardening practices, plant availability and selection) that can greatly influence bee populations by determining the overall amounts of their preferred floral resources [28].In this way, [16] reported 12 botanical families represented by only one species while [14] mention 30 families with only one species.It must be remembered for gardening in a bee friendly purpose that botanical diversity of ornamental plants is a major fact to attend a bigger diversity of bee species.
In relation to the habitus of the plants, in descending order of frequency, are herbs (48.5%), shrubs (21.5%), trees (16.5%), vines (10.5%) and sub shrubs (3%) (Figure 4).According to [29], ornamental plants, in terms of biological properties and agrotechnical requirements, are divided into several groups such as trees, shrubs, perennials, biennials, annuals, grasses and bulbs and their use in beekeeping requires research work for being widely recommended.As shrubs and herbs are the kind of plants more often used in gardening [9], both trends go in the same direction, enhancing the possibilities of implementing bee friendly gardens.
In terms of color of the flowers, predominate, in descending order, the white flowers (69 species), yellow (30), red (26), pink (25), lilacs (15), blue (15), orange (10), purple (9) and green (2) (Figure 5).These findings follow the general tendencies of flower color preferences of bees (bright white, yellow, blue or violet or those that reflect ultraviolet light), described by authors such as [30] and [31], among others.As the color of the flowers have, many times, some relation to the botanical family they belong to [27], the knowledge of the bees' preferences for these taxa should be in mind, in landscaping practices aiming succession of colors in gardens following the seasons.J. Koenig (naturalized) (Zingiberaceae) (6) and Brachyscome multifida DC (endemic) (Asteraceae) (5).According to [20], native bees use a wide variety of ornamentals and their abundance depend on the plant type.Exotic taxa found corroborate studies conducted in Brazil and other countries about the presence of introduced/invasive/naturalized plant species, which insert in the environments where they penetrate and with which native bee species interact [32].Despite the fact that most gardens use a high percentage of nonnative plants (instead of the native plants preferred by native bees), they are nonetheless visited by native bees [28].As stated by [33], a garden plant need not be native to attract and feed native bees.
The results show a large botanical diversity, demonstrating the varied possibilities of utilization of ornamental plants as bee pasture species in urban beekeeping (Figure 6).The botanical families that had more ornamental bee plant species are those that encompass more taxa and so their ratio reflects their taxonomic richness too [34].On the other hand, the fact that there is a proportion of endemic ornamental bee species adds an element of potential economic importance to the issue in focus since the production of ornamental plants is a booming economic activity in Brazil [35].The prevalence of colors of flowers/inflorescences preferred by bees is reported by other authors [14] and should be considered when implementing urban gardening and landscaping for pollinators.

Conclusions
Even though urbanization has a negative effect on insect fauna, wild bees are found in urban environments [36].Urban bees are those that lived in an area prior to urbanization and are able to adapt to anthropogenic alterations to the environment besides the exotic species that have become naturalized therein [20].On the other hand, in urban environments, botanical species with different flowering periods are usually used in gardening, which favors the ornamentation factor [37] and, consequently, the supply of resources is maintained throughout the seasons.Urban plants also are usually intensively managed: watering, pruning and replanting produces floral resources that are more consistently available to pollinators, even in times of drought [20].In urban environments, temperature is a little higher than outside city and pesticides are of restricted use in there [4].
Ornamental plants are not often thought as bee plants because they do not always offer conspicuous pollen or nectar resources [38].Moreover, frequent attributes of ornamental plants such as double petals, no stamens, no nectar guides, strong scents, among others, drive off bees [39].However, many of them are suitable for bees that visit them prominently.Nowadays there is a tendency of consumers for ornamental plants with sustainable attributes [40].So, studies made up about the relations between flowers and native bees, summarized into lists of ornamental bee plants, can allow gardens to be planned to attract them.The potential consequences of pollinator decline on the preservation of biodiversity and stability of food crop yields should guide the policies of pollinator conservation [41]. of the Botanical Museum of the City of Curitiba, for their assistance in botanical identification.To all those who contributed to this work.

Figure 1 .
Figure 1.Flow chart of selection of ornamental bee plants of Santa Catarina State.

Figure 2 .
Figure 2. Quantity of ornamental bee plants species per botanical families, in Santa Catarina State, southern Brazil.

Figure 3 .
Figure 3. Quantity of ornamental bee plants species per botanical genus, in Santa Catarina State, southern Brazil.

Table 1 .
List of ornamental bee plants in Santa Catarina State, southern Brazil.References of this table are after the table.