THE POTENTIAL IMPORTANCE OF SYNANTHROPIC VEGETATION TO BUMBLEBEES IN URBAN ECOSYSTEMS ON THE EXAMPLE OF LUBLIN

This study was an attempt to show synanthropic phytocoenoses of the city of Lublin which are potentially valuable to pollinating insects such as bumblebees. B. terrestris and B. lapidarius as well as B. lucorum, B. hypnorum and B. pascuorum were found to occur in Lublin. Artemisio-Tanacetetum, Bunietum orientalis, and Berteroëtum incanae were shown to be most valuable to bumblebees due to a high number of polleniferous and nectariferous species in these communities. The present study also allowed us to determine that the size of communities and their occurrence in a mosaic with parks and green spaces had an effect on the distribution of bumblebees.


INTRODUCTION
Bumblebees belong to the family Apidae, tribe Bombini.In Europe 62 species are encountered [1], whereas 31 species belonging to the genus Bombus Latreille 1802 have been recorded in Poland [2].Currently, most bumblebee species are fully protected in our country and only the buff-tailed bumblebee and red tailed bumblebee are partially protected under the relevant Regulation of the Minister of Environment [3].Various authors stress the decrease in species richness and in the number of pollinating insects, including bumblebees [4][5][6][7][8][9].
Bumblebees occur in different environments, including urbanized environment [10][11][12][13][14][15][16][17][18].Some forms of urban green spaces can be important resources for pollinators [14,19,20].Even roadside vegetation can play a major role in the development of pollinating insects [21].Many insects, including pollinators, use synanthropic plants as a source of food [5,7,[22][23][24][25].The importance of green areas as local fauna habitats is also increasing [17].Even a small space overgrown with synanthropic vegetation is sometimes sufficient and can become a refuge for insects [26][27][28].As reported by B a n a s z a k [29], a large dominance of social bee species is observed in cities.This author supposes that the social life of bees can be instrumental in overcoming the barriers of urbanization, similarly as polylectism, that is, an adaptation to forage on flowers of many unrelated plant species [5,29,30].Bumblebees are both social and polylectic bees and hence they have traits that facilitate their survival in the anthropogenic environment.Nevertheless, A h r n é et al. [31] found in Stockholm a decline in the numbers of bumblebee species along a gradient of increasing urbanization, even in the case of the presence of a suitable habitat for foraging.In turn, P a w l i k o w s k i and O l ę d zk a [32] showed in Toruń that the mosaic nature of habitats and the proportion of developed land had the greatest effect on the occurrence of bumblebees in this city.Bumblebees prefer habitats with a large proportion of shrubs and in which developed land does not exceed 40% of the area [32].Bumblebees build their nests mostly in the soil, but also on its surface between stones and plants, or in leaf litter.Most nests are observed on the edges of forests and tree stands as well as under shrubs, in field margins or in clover crops [5,7].Both foraging flight ranges and energy requirements of large and small bees differ [33,34].
As a result of that, each of these groups responds differently to environmental changes at the landscape level.Their sensitivity to the specific characteristics of a particular habitat also varies [35,36].Large social bees, including bumblebees, are capable of foraging within a radius of more than 1 km from their nests, whereas smaller solitary bees are generally thought to be able to fly to a distance of about 250 m from their nests [20,34,37,38].However, E r e m e e v a and S us h c h e v [25] report that bumblebees look for food within a radius of 2 km from their nests.In turn, W o l f and M o r i t z [39] showed that Bombus terrestris workers foraged within an average distance of 267 m from their nests, 800 m at the maximum.G r e e n l e a f et al. [34] give a method for measuring foraging distance of Apidae depending on body size, but the presented results mainly relate to non-social bees.However, these authors did not determine whether trophic specialization (including polylectism) affected bee foraging distance [34].
In the Lublin region, there have been earlier studies on the importance of plants to pollinating insects.M a s i e r o w s k a [40] studied in Lublin ornamental plants of the family Saxifragaceae as a source of food for pollinating insects.W r z e s i e ń and D e n i s o w [26,41,42] investigated the proportion of bee plants in xerothermic grasslands of the Lublin Upland and in phytocoenoses near railway tracks of the Lublin Upland as well as in the Roztocze and Polesie regions.D e n i s o w and W r z e s i e ń [43] investigated midfield tree stands, fallow lands and field margins in the area of Lublin, with special attention to nectariferous and polleniferous plants.
The aim of the present study was to show the role of synanthropic communities to bumblebees found in urbanized areas on the example of Lublin.Biodiversity conservation provides for measures at all levels and in all kinds of environments.Therefore, the present authors decided to investigate the potential importance of spontaneous vegetation of urban areas in the maintenance of biological diversity of this important group of pollinating insects, notably bumblebees.

MATERIALS AND METHODS
Phytosociological surveys covering the Lublin city area formed the basis for this study designed to determine the importance of synanthropic vegetation to bumblebees.386 relevés were made over the period 2005-2010.Field investigations were carried out using relevés which were analysed following the Braun-Blanquet method.During the investigations, bumblebee visitation and foraging were observed.In May and June 2012, observations were carried out in individual synanthropic communities to record in which of them bumblebees appeared and in which they did not occur.
These were only qualitative investigations, not quantitative ones.Particular individuals were not counted and only the presence of bumblebees in a particular type of environment was recorded.This allowed us to initially determine whether synanthropic communities of Lublin were used by bumblebees at all.Bumblebees were identified using the relevant keys [7,44].
Subsequently, the collected material was analysed in terms of the potential usefulness of the identified communities and plants composing these communities to bumblebees.The distribution and size of synanthropic vegetation patches in Lublin were analysed.Synthetic vegetation tables were made and they showed the following indices: cover-abundance, sociability and constancy.The phenology of synanthropic plant species occurring in synanthropic communities of Lublin was determined.The data relating to plants useful to pollinating insects (nectariferous and polleniferous species) followed [26,45].The obtained phytosociological data were compared with the phenology of the two most frequently observed bumblebee species, Bombus terrestris and Bombus lapidarius.In this way, the study demonstrated the potential usefulness of synanthropic plant communities in Lublin as a food resource for bumblebees.This paper follows phytosociological nomenclature of M a t u s z k i e w i c z [46] and it is additionally based on the studies of F i j a ł k o w s k i [47] and J a n e c k i [48].The names of bumblebees follow B a n a s z a k [2].

RESULTS
The present study conducted in Lublin found the occurrence of 35 1).
The presence of bumblebees was recorded in most synanthropic communities of Lublin.These insects were not observed only in the community with Lepidum ruderale, Chenopodietum stricti, Panico--Eragrostietum, and Bryo-Saginetum.The following bumblebee species were found to occur within the study area: Bombus terrestris (Linnaeus 1758), Bombus lapidarius (Linnaeus 1758), Bombus lucorum (Linnaeus 1761), Bombus hypnorum (Linnaeus 1758), and Bombus pascuorum (Scopoli 1763).The other bumblebees that appeared within the study area were not identified to the level of species.Two species: B. terrestris and B. lapidaries, were most frequently observed.Given that bumblebees foraging in synanthropic communities were observed in Lublin, it should therefore be assumed that a part of them can also nest within the city area, including in synanthropic communities where shrubs or clusters of plants such as Tanacetum vulgare are observed.
The pattern of distribution and variation of synanthropic communities in Lublin can be related to the occurrence of bumblebees.These insects are associated with areas in which they can build nests and at the same time find food [49,50].As shown by the research, the spatial pattern of communities is determined by anthropogenic factors manifested in the zonation from the centre of the city to its outskirts and this is associated with the historically determined distribution of anthropopressure.Different zones can be distinguished, which is also confirmed by the study on vegetation conducted by R y s i a k [51].
The smallest spaces are occupied by synanthropic plants and communities in the city centre where at the same time green areas are also the smallest.They are limited to degraded lawns and slopes.There are communities with low specialization (Lolio-Polygonetum, Bryo-Saginetum procumbentis, a community with Lycium barbarum), communities in impoverished form (a smaller number of species recorded in these communities compared to those found on the city outskirts), and communities that often occur only temporarily (Panico-Eragrostietum), which is associated with their destruction during tending treatments.Single bumblebee individuals were observed there, in particular on the slope of the Old Town near allotment gardens located on the Bystrzyca River.
The variation in plants and communities increases with an increasing distance from the city centre and already in the Śródmieście district synanthropic communities occupy larger area; apart from the above--mentioned ones, communities associated with parks, green spaces, and flower borders appear (Galinsogo--Setarietum, Urtico-Malvetum, Hordeetum murini, Urtico-Aegopodietum, a community with Impatiens parviflora, Chelidonio-Robinietum).Here, there are also no connections between individual spaces overgrown with plants.As indicated above, single bumblebee individuals were recorded in these communities.
On the other hand, in housing estates, near roads and on bodies of water, synanthropic plants and communities are an admixture and they form a mosaic together with structured vegetation and natural communities.In terms of area, synanthropic communities are a dominant component of green spaces (extensive lawns).23 synanthropic communities were identified in this part of the city.Among them, the following were frequently encountered: Bunietum orientalis, Cardario-Agropyretum, Chelidonio-Robinietum, and Urtico-Aegopodietum.They usually develop near cultural landscape elements: consciously structured plant cover or artificial abiotic structures.This variation in communities and the occurrence of a mosaic had a distinct effect on the presence of bumblebees, in particular at places where wastelands and extensive lawns were adjacent to each other.
Synanthropic communities are a major element of the landscape in undeveloped areas and wastelands.Communities found in such places are characterized by high species variation and they occupy an area from 25 m, to several hectares [52].For many years, the development of ruderal communities has been observed near railway tracks and in post-industrial areas that have not yet been designated for any specific use as well as in managed green spaces such as lawns and parks.Such wastelands overgrown primarily with Artemisio-Tanacetetum can be found in almost all the gullies of Lublin, but also in fallow lands in a mosaic with cultivated fields on the city outskirts.Ruderal communities also occupy the largest areas in Lublin, though the spread of these communities is limited by changes in land use, progressive urbanization, the development of wastelands, and the aestheticization of space.Bumblebees were most often observed in such places and these were always numerous individuals.
In Lublin the variation of synanthropic communities and the area occupied by them affected the occurrence of bumblebees.This is also shown in the research of P a w l i k o w s k i and O l ę d z k a [32] as well as in the study of E r e m e e v a and S u s h c h e v [25].Bumblebees prefer urban areas with mosaic vegetation, but with a predominance of shrubby vegetation, and they nest within a distance of 2km from foraging sites.They choose areas with woody or grassland vegetation much less frequently [25,32].To build nests, bumblebee species occurring in Poland need areas covered by shrubs or with dense canopies of large perennials.A part of species nest on the edges of tree stands [5].Only some species, such as Bombus hypnorum, are able to locate their nests in gaps between stones or in attics of residential and industrial buildings [25].
Spontaneous synanthropic communities develop to different degrees and their floristic composition significantly differ from the structure of communities known from typical ruderal sites (wastelands, landfills, places near human dwellings and fences, etc.) in, among others, the proportion of meadow species and in the absence of characteristic synanthropic species.
The analysis of the status of synanthropic communities in Lublin shows that urbanization results not only in decreased variation in plant communities, but it also causes a decline in the number of species.Resistant species, in particular cosmopolitan ones (Eragrostis sp., Plantago major, Polygonum aviculare), which form small clusters and are of little importance to bumblebees, are predominant in the city centre.The further from the centre, the variation in anthropopressure forms increases the richness of plant communities and the number of species in the external zone of Lublin also increases.In terms of species variation, the least numerous were associations of the class Molinio-Arrhenatheretea -Bryo-Saginetum in which 17 species were identified (on average 4 species per relevé) and of the class Stelarietea mediae -a community with Lepidium ruderale, in which 11 species were identified (on average 7); they were found in habitats most transformed by anthropopressure in the city centre.The following communities of the class Artemisietea vulgaris were richest in species: Artemisio-Tanacetetum in which 170 species were found (on average 17) and Bunietum orientalis with 110 species (on average 18), occurring in the gullies, wastelands, and extensive lawns.These are also communities richest in nectar and pollen producing species (Table 1).The largest concentrations of bee plants were found in the following communities: Atremisio-Tanacetetum (60 species), Bunietum orientalis (46 species), and Berteroëtum incanae (41 species).Half less polleniferous and nectariferous species were found in the following communities: Sisymbrietum loeselii (27 species), Urtico-Calystegietum (21 species), Urtico-Malvetum (20 species), Echio-Melilotetum (20 species), and Leonuro-Ballotetum (20 species).The percentage of bee forage species found in individual communities is from 14 to 100%, whereas in nine communities they accounted for more than 50% of the species composition.However, this does not coincide with the variation in the communities in terms of their species richness.In spite of great species variation in synanthropic communities, only a part of plant species important to bumblebees occur frequently or with high cover-abundance and sociability in synanthropic communities of Lublin, which was determined taking into account the constancy classes (Table 2).The following can be mentioned among them: Achillea millefolium L. (17 associations), Aegopodium podagraria L.  10associations).At the same time, it was observed that there were communities, e.g.Erigeronto-Lactucetum, Panico-Eragrostietum, Ivetum xantifoliae, and a community with Impatiens glandulifera, in which bee plants were most frequently characterized by low cover.Besides, the species found in them do not provide for the needs of insects throughout the whole season.
Another aspect that was taken into consideration was the flowering duration of bee plants in particular communities and clusters formed by them.The analysis of the presence of bee forage plants in particular communities and their flowering periods shows that the above-mentioned plants formed dense clusters and their flowering occurred in different periods of the growing season in the following communities: Atremisio--Tanacetetum, Bunietum orientalis, and Berteroëtum incanae (Tables 2 and 3).
The results of the present study compared with the phenology of the two most numerous bumblebee species confirm the potential usefulness of synanthropic plant communities to these insects.In particular, the flowering periods of synanthropic bee plants clearly coincide with the periods of dynamic bumblebee development (Tables 2-4).Plants of synanthropic communities such as Tussilago farfara or Trifolium repens flower already from April or May.In turn, Ballota nigra and Medicago sp.flower from June even until the end of September (Table 2).The strongest bumblebee colony development usually occurs between June and August (Table 4), which coincides with the flowering of many plants valuable to these insects or of one species but which is a dominant element in the community.It is perfectly reflected in Table 3 which shows the flowering of bee plants in synanthropic communities of Lublin.The dominant (full) flowering occurs in particular in June, July and August, thus in the months important in bumblebee colony development.Taking into account both the number of bee forage species in synanthropic communities of Lublin and the full flowering period of these plants, it can be stated that the communities Artemisio-Tanacetetum and Bunietum orientalis have the greatest importance as a source of food for bumblebees, even more so that these communities occupy larger areas and occur in a mosaic with other communities.We should not however ignore the importance of other communities that can be a supplementary source of food, since bumblebees are polylectic insects.Given the trophic adaptations of bumblebees, it can be concluded that synanthropic communities are potentially very valuable to them.In the spring and early summer, these insects readily visit flowers of trees such as Robinia pseudoacacia or Tilia cordata as a source of food, but the period of late summer or early autumn is not abundant in flowering trees and therefore species such as Galium aparine or Lamium album have a huge role in providing food to bumblebees after these trees finish flowering.
As mentioned above, it is presumed that polylectism of bees, i.e. visiting flowers of unrelated plants, is also an important feature that facilitates their survival in the anthropogenic environment [30].B an a s z a k -C i b i c k a [30] includes Apis melifera L. and members of the genus Bombus in bees characterized by polylectism.Thus, given that bumblebees can collect food from many unrelated plants, a conclusion then arises that such species-diverse synanthropic communities of Lublin have a major role for bumblebees.
Bumblebees are very efficient pollinators and besides they are less sensitive to changes in atmospheric conditions than A. melifera, especially to a decrease in temperature and an increase in air humidity.It is presumed that the work of one bumblebee is equal to the work of 4-5 honey bee workers [5].The role of bumblebees as pollinators in human economy and in the maintenance of the diversity of entomophilous flora is invaluable and therefore it seems so important to maintain the largest possible number of environments that they can inhabit.The phenomenon of mass die-off of A. melifera, termed the CCD (Colony Collapse Disorder) syndrome, has been observed in the world since 2006.Over a period of 4 years, the numbers of bees in Germany and France decreased by 40%, while in some regions of the USA even by 90%.In Poland this phenomenon is not observed with such intensity, but the first symptoms can already be noticed [58].Therefore, apart from the research designed to find the reasons for the CCD syndrome and to prevent it, simultaneously it is important to protect pollinators, including bumblebees.
It is worth maintaining habitats that will serve bumblebees in their development.The importance of urban areas as unique fauna reservoirs is continually increasing [14,17].Under the Convention on Biological Diversity, biodiversity conservation is included in the state's tasks and hence it is also important to protect ecosystems and the continuity of biological process in cities. Cities do not have vast habitat areas and in cities there are few such biologically diverse places as synanthropic communities.In wasteland, animals can find breeding sites and valuable trophic areas, since well--tended green spaces will not play such a role.Most bumblebee species found in Poland build their nests in the soil [5,7].It is not possible for them to locate their nests in intensely mowed lawns or carefully tended flower borders.Therefore, synanthropic communities have a major role to play again; as natural open areas, they can be perfect habitats for bumblebees.
The maintenance of spontaneous synanthropic vegetation in urban areas enables the conservation of biodiversity at different levels and leaving these habitats creates conditions for living and development of many animal species, including useful and protected species such as bumblebees.

Table 1
Species variation in synanthropic communities found in Lublin, together with the number and percentage of bee plant species

Table 2 .
List and characteristics of plant species most frequently found in synanthropic communities in Lublin