Skip to main content

Variability of bumblebee communities (Apidae, Bombini) in urban green areas

Abstract

Based on current research the agglomerations are potentially desirable habitats for bumblebees. However, the relationship between the biodiversity of these bees and the green areas where they live is poorly understood. The aim of the study was to estimate the influence of green areas (ranging from 8 to 102 ha) of big cities on bumblebee species richness, composition, and the relative number of these insects. The studies were conducted within the administrative borders of the city of Wrocław (Poland) in 2011–2012 in 12 green areas such as parks, cemeteries and other places with trees and shrubs. Species richness and abundance of bumblebees was determined by direct observation during 30 min. The gathered materials were used to calculate how areas of urban green space affected qualitative and quantitative bumblebee community structure. In total, 13 species of bumblebees (Bombus Latr.) were recorded, of which 3 belonged to cuckoo bumblebees (Psithyrus subgenus). The share of the most similar groups was congregated in green areas not smaller than 30 ha. This was proved by analysis of qualitative structure (Sørensen index), quantitative structure (Renkonen index), and qualitative-quantitative structure (Cody’s index). The number of bumblebee species in the surveyed green areas (r = 0.7497) was decisive for the arrangement of the mutual similarity of group structure. Green urban areas should be created in a size of at least 30 ha. Such sites provide conditions for the most diversified bumblebee species communities. Sites smaller than 30 ha can play an important role as refuges, and allow migration to all pollinators.

Introduction

Both in Poland and in other European countries, there has been a continuous decline in bumblebees and their habitats, starting from the 1980s. The main reasons for this are: the loss and fragmentation of habitats, pesticide usage, disease, parasites, non-native species, climate change, and the interaction between these factors. This situation could cause serious disruptions in the functioning of nature, and economic losses as bees are important pollinators. It is estimated that 35% of the world’s food supply entirely depends on these insects (Klein et al. 2007; Potts et al. 2010).

Bumblebees are particularly important pollinators in greenhouses, e.g. tomatoes. They are also specialized, unlike some other bee species, in causing the flower to vibrate – the phenomenon known as buzz pollination. Moreover, a large number of plant species are mainly or exclusively pollinated by bumblebees. This generates a strong relationship between the survival of plant species and bumblebees’ presence (Corbet et al. 1991). At a moment when a particular insect “vanishes” from the habitat occupied by a plant community the “domino effect” starts, which impacts herbivores and other dependent animal species (Corbet et al. 1991; Goulson 2010; Goulson et al. 2005; Pawlikowski et al. 2016).

In the face of the decreasing amount of agricultural areas suitable for bumblebees, the urban environment is gaining growing interest in the context of their active protection (Goddard et al. 2010). The attractiveness of urban green areas for sustaining diverse resources for bumblebees was recorded in parks in San Francisco (McFrederick and LeBuhn 2005) and suburban areas in Great Britain (Goulson et al. 2002; Osborne et al. 2008).

Cities, from the ecological point of view, are a unique mosaic of habitats with residential, commercial, industrial and infrastructure character, among which there are green areas (Breuste et al. 2008). The green areas of a city are very diverse, and apart of man-made gardens or parks, there are also enclaves of natural and semi-natural plant communities (Chudzicka et al. 1998) with characteristic sets of plant and animal species (Niemela 1999). The essential condition for the bumblebees’ occurrence, regardless of the habitat type, is the availability of food sources (Alford 1975). Therefore, a special role in urban areas is attributed to such green areas, which accumulate vast numbers of flowering plants. The primary, but not the only factor which affects the abundance of bumblebees, is flora richness (Widmer and Schmid-Hempel 1999; Steffan-Dewenter et al. 2002; Diaz-Ferero et al. 2012; Sikora and Kelm 2012; Sikora et al. 2016). It also turns out that not only do habitat characteristics have an impact on bumblebees biodiversity, but also factors in the spatial landscape scale, such as the areas which surround particular habitats (Hatfield and LeBuhn 2007). In the mosaic environment of a big city the attractiveness of green spaces should also be determined by their areas. So far, this relationship has not been strictly defined (Hatfield and LeBuhn 2007; Bates et al. 2011).

The aim of the study was to estimate the influence of the green spaces of big cities on bumblebee species richness, composition, and the relative number of bumblebee communities in Wrocław.

Materials and methods

The study was conducted in 2011 and 2012 on 12 sites of Wrocław (Poland) green areas. These areas, ranging from 8 to 102 ha, were parks, cemeteries, railways and wasteland (Fig. 1). Habitats in each surveyed area were mainly formed by trees and shrubs.

Fig. 1
figure1

Dispersion of sites in the Wrocław area: C1 – Grabiszyński Cemetery, C2 – Osobowicki Cemetery, P1 – Szczytnicki Park, P2 – Tysiąclecia Park, P3 – Zachodni Park, P4 – Grabiszyński Park, P5 – Południowy Park, P6 – Wschodni Park, R1 – Strzegomska Railway, R2 – Żernicka Railway, W1 – Mikołajskie Wasteland, W2 – Gajowe Wasteland

Species richness and abundance of bumblebees were determined by direct observation during 30 min (= sample). Observations were conducted once per month between March and September, from 10:00 am to 5:00 pm, in favourable weather conditions for bee flights (Pawlikowski 2010). Bumblebees were counted on visited plant species. Specimens of Bombus terrestris and Bombus lucorum were counted together, as it is hard to distinguish between them during field surveys. Individual specimens of workers and males castes, impossible to identify in the field, were caught and euthanized with ethyl acetate (method approved by the Regional and General Director of Environmental Protection in Poland for 2011–2012). The specimens are stored in the Department of Plant Protection, the University of Life Sciences, Wrocław.

The gathered materials were used to identify the structure of bumblebee communities on the study sites. The structure of distanced communities was described using the number of species (S), average density (At), an index of total species diversity (H′), and an evenness index (J’). Average density (At) was the number of recorded specimens on the site per 30 min of observation. The Shannon and Weaver (1963) was used as a formula to calculate the index of general species diversity. The evenness index of species frequency distribution was calculated using Pielou (1966). The qualitative similarity of the distanced communities (QS) was calculated using the Sørensen (1948), while quantitative similarity (Re) was determined by using the Renkonen (1938). Cody (1970) was used for quantitative and qualitative comparisons of bumblebee communities. The QS and Re indices were selected in order to assess the similarity of the communities according to their adequate representation of species number and density in the communities along an appointed gradient of the surveyed areas’ size. The qualitative and quantitative similarity of habitats was calculated using the MS EXEL program, and the graphic file was generated in PHOTOSHOP CS6 software. Specific structure parameters (S, At, H′, J’) were additionally surveyed in terms of the relationship with the size of the habitats. Structure parameters were calculated according to correlation analysis, with a significance level of p ≤ 0.05. Calculations were made with STATISTICA v 6.0 software. In order to define the surveyed site areas the Wrocław Map of Geographic Information System was used, together with measuring applications available at: www.geoportal.wroclaw.pl.

Results

In the 12 surveyed habitats 14 species of bumblebees (Bombus Latr.) were recorded, in which 3 belong to cuckoo bumblebees (Psithyrus subgenus) (Table 1). In Szczytnicki Park (P1) the highest number of bumblebee species (12) was observed, whereas the lowest species number (5) was recorded on Gajowe Wasteland (W2) and Żernicka Railway (R2).

Table 1 Parameters of bumblebee communities in Wrocław green areas in the phenological seasons 2011–2012

The highest average density of bumblebees (At) was recorded in the Gajowe Wasteland area (W2) – 68.5 specimens/30′, while the lowest occurred in the Zachodni Park area (P3) – 13.42 specimens/30′.

On the qualitative diagram (Fig. 2), based on the Sørensen index of species similarity (QS), 7 communities with predominant mutual similarity above 77% were distanced. Those communities were present on the surveyed sites above 30 ha. The other 5 communities, within smaller areas P2, R2, R1, W1 and W2, showed lower mutual similarity. Amongst them, the smallest similarity to the others (less than 50%) was characteristic for the community in area R2.

Fig. 2
figure2

Diagrams of qualitative similarity (QS) and quantitative similarity (Re) of bumblebee communities according to the gradient of green areas in Wrocław

On the quantitative diagram (Fig. 2), based on the Renkonen index (Re), 7 communities with area above 30 ha have been extracted. Among all of the other sites smaller than 30 ha, the most similar community was for the R1, W1 and W2 areas.

On dendrite resemblance based on the qualitative-quantitative Cody’s index (Fig. 3), bumblebee communities clearly concentrate in regard to P6 and C2 communities. Within the range of average T value there are 7 communities from the sites of 30 ha area each.

Fig. 3
figure3

Dendrite resemblance presenting species diversity of bumblebee communities in green areas of Wrocław. The communities refer to the circle of Cody’s index average values (T)

Analyses of communities structure dependence parameters indicated a strong positive correlation between the number of bumblebee species (r = 0.7497) and the size of urban green areas. In the case of species diversity (r = 0.3566) and evenness (r = 0.0344) there was a weak positive correlation, and for average density (r = −0.2677) a weak negative correlation (Fig. 4).

Fig. 4
figure4

Structure parameters of bumblebee communities according to the gradient of green areas in Wrocław

Discussions/Conclusions

The urban agglomerations might be potentially attractive habitats for bumblebees thanks to the mosaic of green areas. In the spatial plan of Wrocław the green spaces are formed in annular-cuneiform, enabling their permanence, which positively influences the entirety of natural factors (Bińkowska and Szopińska 2013). The green areas of Wrocław constitute a fifth of the total city area, and within the city borders there are zones of the European Natura 2000 network.

According to Alford (1975), bumblebee species richness in different areas depends on the food attractiveness of these habitats, and thus the areas with the highest number of bumblebee species must be characterized by specific features. Such a place in Wrocław is Szczytnicki Park, the oldest and largest urban park. Moreover, it was the only area where a bumblebee rare in the country and on the European scale, Bombus humilis, was found.

The factor affecting the number of bumblebee species on Wrocław sites was the area of the green areas. This confirms the assumptions of the theory of insular biogeography (MacArthur and Wilson 1967). The theory states that the bigger the area of habitat, the more bumblebee species can be expected there. Analogical conclusions were drawn in relation to birds (Evans et al. 2009), amphibians (Parris 2006), mammals (Magle et al. 2009), and ground beetles (Sadler et al. 2006) living in urban habitats, and bumblebees living in meadow habitats of the rural landscape (Diaz-Ferero et al. 2012).

During research into bumblebees in Estonia, where the size of rural areas was correlated with the bumblebee numbers, it was pointed out that the bigger the size of a rural farm, the lesser the bumblebee number (Muljar et al. 2010). The above-mentioned theory of insular biogeography explains the matter of the numbers in a way that in a bigger area the specimen dispersion is greater (MacArthur and Wilson 1967). However, the research carried out in urban habitats, like urban gardens and traditional flowerbeds in many kinds of green spaces, does not demonstrate the impact of the area site on bumblebee numbers (Gunnarsson and Federsel 2014). Also, during the surveys undertaken on the Wrocław sites the impact of the site area on bumblebee numbers was not observed.

Other researchers point out that floristic richness is a factor influencing the bumblebees abundance and their species diversity (Widmer and Schmid-Hempel 1999; Steffan-Dewenter et al. 2002; Diaz-Ferero et al. 2012; Parde and Philipott 2014; Salisbury et al. 2015; Wood et al. 2015). However, on the Wrocław study sites the number of visited flowering plants did not correlate with the size of the site r = 0.0792 (Fig. 5). Therefore, the quality factors like the degree of food attractiveness and abundance in the habitat seem to be more important than the number of flowering plants. The bumblebees abundance depends primarily on the quality, availability and stability of food sources in the inhabited area. Comparing the bumblebees’ density in urban parks, cemeteries and allotments, the highest value was presented in species-rich flower gardens (Ahrne 2008). In such places, with a high diversity of flowering plants, bumblebee density can reach 8 specimens per 100 m2 (Matteson and Langellotto 2009), while on cultivated fields in England only 4–5 specimens per 100 sq. m (Carvell et al. 2004) and less than 1 specimen on 100 sq. m on meadow habitats in Sweden (Öckinger and Smith 2007). Observed trophic interactions confirm the principle that a few but adequately selected plant species as food sources might provide suitable conditions for the development of numerous bumblebee families. This has significant importance in rural environments, where the economic use of bumblebees is mainly focused on plant monocultures (Goulson 2010).

Fig. 5
figure5

Relationship between the number of visited flowering plants (P) and the size of green areas in Wrocław

Isolation in extremely fragmented city habitats is a serious threat for bumblebee families. Smaller populations are more vulnerable to extinction due to environmental changes (Frankham et al. 2002). It was confirmed that populations which cannot freely move between habitats are forced to inbreed, and this leads to a decrease in the condition of the whole population (Krebs 2009). Habitat fragmentation may cause a situation where too small sites with food plants will not be attractive for some bumblebee species (Mayer et al. 2012).

Within the city space the sequences of green areas along roads should allow migration. In the Wrocław agglomeration such a function can be fulfilled by railway sites with attractive ruderal plants. Plants from the Fabaceae family could be a perfect pollen source for visiting bumblebees (Goulson and Darvill 2004). The value of these sites is undoubtedly increased by the presence of one of the rarest and endangered bumblebee species in Poland – Bombus veteranus.

International efforts to preserve the environment are focused mainly on large ecosystems, usually very little altered by human activity. Less attention is paid to small green spaces in cities, in neighbourhoods where people live and work. However, urban parks and open green areas are essentially important for the quality of life in a more urbanised society (Chiesura 2004). The protection of the wild bee population makes sense only when it is carried out on a landscape scale, which requires coordination and cooperation at a regional level (Richards 1993). The first step towards effective management in the urban environment is the recognition of landscape factors on a patch scale, which affects biodiversity (Angold et al. 2006). The next step is to tackle a social challenge – combining the practice of management with the achievements of scientific theories (Cadenasso and Pickett 2008). Considering the obtained results, large green urban areas should be created of a size of at least 30 ha. Such sites are similar to each other in terms of habitat attractiveness and provide conditions for the most diversified bumblebee species communities.

Such sites will be pollinator shelters if managed properly. In the most potentially attractive habitats mowing, and herbicide and insecticide usage should be restricted. On lawns and green spaces with blooming clovers (Trifolium spp.), birdsfoot trefoil (Lotus corniculatus), self-heals (Prunella spp.) and knapweeds (Centaurea spp.), the maintenance treatments should consider the appropriate height of cutting, providing constant flower food sources. For urban parks special management plans should be developed in order to determine the rules of habitat use which consider the active protection of pollinators. Margin areas with shrubs, tall grass and touchwood should be in every park as nesting habitats for pollinating insects. In order to increase the potential of lawns and green spaces, mixes of native flowering species should be introduced in the form of blooming stripes and flower rich meadows. In habitats such as urban parks, which are used for recreation and sport, an effective solution would be the introduction of flowerbeds, which are attractive for bumblebees. The flowerbeds, including native and exotic plant species, would play a natural, aesthetic and educational role.

On sites smaller than 30 ha the bumblebee communities were dominated by abundant species with a wider polyphagous spectrum. However, small green areas can play an important role as refuges and allow migration to all pollinators, especially when places are enriched with a mosaic of various food plants. In each habitat it is possible to introduce even small alterations beneficial for pollinators. Undoubtedly, the protection strategies should be mainly based on blooming species diversity and richness (Sutcliffe and Plowright 1988).

References

  1. Ahrne K (2008) Local Management and Landscape Effect on Diversity of Bees, Wasps and Birds in Urban Green Area http://pub.epsilon.slu.se/1766/1/Kappan.pdf. Accessed Aug 2016

  2. Alford DV (1975) Bumblebees. D. Poynter, London

    Google Scholar 

  3. Angold PG, Sadler JP, Hill MO, Pullin A, Rushton S, Austin K, Small E, Wood B, Wadsworth R, Sanderson R, Thompson K (2006) Biodiversity in urban habitat patches. Science Total Envir 360:196–204

    CAS  Article  Google Scholar 

  4. Bates AJ, Sadler JP, Fairbrass AJ, Falk SJ, Hale JD (2011) Changing bee and hoverfly pollinator assemblages along an urban–rural gradient. PLoS One 6(8):e23459

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. Bińkowska I, Szopińska E (2013) Leksykon zieleni Wrocławia. Via Nova, Wrocław

    Google Scholar 

  6. Breuste J, Niemela J, Snep RPH (2008) Applying landscape ecological principles in urban environments. Landsc Ecol 23:1139–1142

    Article  Google Scholar 

  7. Cadenasso ML, Pickett STA (2008) Urban principles for ecological landscape design and management: scientific fundamentals. Cities Envir 1(2):1–16

    Article  Google Scholar 

  8. Carvell C, Meek WR, Pywell RF, Nowakowski M (2004) The response of foraging bumblebees to successional change in newly created arable field margins. Biol Conserv 118:327–339

    Article  Google Scholar 

  9. Chiesura A (2004) The role of urban parks for the sustainable city. Landscape Urban Plann 68:129–138

    Article  Google Scholar 

  10. Chudzicka E, Skibińska E, Winiarska G (1998) Zasiedlenie środowiska miejskiego przez owady (Settlement of the Urban Environment by insects) In: Barczak T and Indykiewicz P (ed) Fauna miast (Urban fauna). Wyd. ATR, Bydgoszcz, pp 47–55

    Google Scholar 

  11. Cody ML (1970) Chilean bird distribution. Ecology 51:453–464. doi:10.2307/1935380

    Article  Google Scholar 

  12. Corbet SA, Williams IH, Osborne JL (1991) Bees and the pollination of crops and wild flowers in the European Community. Bee World 72:47–59

    Article  Google Scholar 

  13. Diaz-Ferero I, Kuusemets V, Mand M, Liivamagi A, Kaart T, Luig J (2012) Influence of local and landscape factors on bumblebees in semi–natural meadows: a multiple–scale study in a forested landscape. J Insect Conserv 17:113–125

    Article  Google Scholar 

  14. Evans KL, Newson SE, Gaston KJ (2009) Habitat influences on urban avian assemblages. Ibis 151:19–39

    Article  Google Scholar 

  15. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Book  Google Scholar 

  16. Goddard MA, Dougill AJ, Benton TG (2010) Scaling up from gardens: biodiversity conservation in urban environments. Trends Ecol Evol 25(2):90–98

    Article  PubMed  Google Scholar 

  17. Goulson D (2010) Bumblebees, behaviour, Ecology and conservation, Second edn. Oxford University Press, New York

    Google Scholar 

  18. Goulson D, Darvill B (2004) Niche overlap and diet breath in bumblebees; are rare species more specialized in their choice of flowers? Apidologie 35:55–63

    Article  Google Scholar 

  19. Goulson D, Hughes WOH, Derwent LC, Stout JC (2002) Colony growth of the bumblebee, Bombus terrestris, in improved and conventional agricultural and suburban habitats. Oecologia 130:267–273

    CAS  Article  PubMed  Google Scholar 

  20. Goulson D, Hanley ME, Darvill B, Ellis JS, Knight ME (2005) Causes of rarity in bumblebees. Biol Conserv 122:1–8

    Article  Google Scholar 

  21. Gunnarsson B, Federsel LM (2014) Bumblebees in the city: abundance, species richness and diversity in two urban habitats. J Incect Conserv 18:1185–1191

    Article  Google Scholar 

  22. Hatfield RG, LeBuhn G (2007) Patch and landscape factors shape community assemblage of bumble bees, Bombus spp. (Hymenoptera: Apidae), in montane meadows. Biol Concerv 139:150–158

    Article  Google Scholar 

  23. Klein AM, Vaissiera BE, Cane JH, Steffen-Dewenter I, Cunningham SA, Kremen C, Tschrantke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B 274:303–313

    Article  PubMed  Google Scholar 

  24. Krebs CJ (2009) Ecology: the experimental analysis of distribution and abundance. University of British Columbia, Vancouver

    Google Scholar 

  25. MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton

    Google Scholar 

  26. Magle SB, Theobald DM, Crooks KR (2009) A comparison of metrics predicting landscape connectivity for a highly interactive species along an urban gradient in Colorado, USA. Landsc Ecol 24:267–280

    Article  Google Scholar 

  27. Matteson KC, Langellotto GA (2009) Bumble bee abundance in new York City Community gardens: implications for urban agriculture. Cities and the Environment 2:1–12

    Article  Google Scholar 

  28. Mayer C, Michez D, Chyzy A, Bre’dat E, Jacquemart A-L (2012) The abundance and pollen foraging behaviour of bumble bees in relation to population size of whortleberry (Vaccinium Uliginosum). PLoS One 7(11):e50353. doi:10.1371/journal.pone.0050353

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. McFrederick QS, LeBuhn G (2005) Are urban parks refuges for bumble bees Bombus spp. (Hymenoptera:Apidae)? Biol Conserv 129:372–382

    Article  Google Scholar 

  30. Muljar R, Viik E, Marja R, Svilponis E, Jõgar K, Karise R, Mänd M (2010) The effect of field size on the number of bumble bees. Agronomy research 8(special issue II):357–360

  31. \Niemela J (1999) Ecology and urban Planing. Biodivers Conserv 8:119–131

    Article  Google Scholar 

  32. Öckinger E, Smith HG (2007) Semi–natural grasslands as population sources for pollinating insects in agricultural landscapes. J Appl Ecol 44:50–59

    Article  Google Scholar 

  33. Osborne JL, Martin AP, Shortall CR, Todd AD, Goulson D, Knight ME, Hale RJ, Sanderson RA (2008) Quantifying and comparing bumblebee nest densities in gardens and countryside habitats. J Appl Ecol 45:784–792

    Article  Google Scholar 

  34. Parde GL, Philipott SM (2014) Native plants are the bee's knees: local and landscape predictors of bee richness and abundance in backyard gardens. Urban Ecosyst 17:641–659

    Article  Google Scholar 

  35. Parris KM (2006) Urban amphibian assemblages as metacommunities. J Anim Ecol 75:757–764

    Article  PubMed  Google Scholar 

  36. Pawlikowski T (2010) Structural dynamic of bumblebee communities (Hymenoptera: Bombini) in forest areas destroyed by acid rains in the Karkonosze Mountains of Poland. J Apic Sci 54(1):35–41

    Google Scholar 

  37. Pawlikowski T, Olszewski P, Żyła W, Przybylińska M (2016) The rare oligolectic bumblebee Bombus gerstaeckeri Morawitz, 1882 from Poland. Spixiana 39(1):130

    Google Scholar 

  38. Pielou EC (1966) Shannon’s formula as a measure of specific diversity: its use and misuse. Amer Naturalist 100:463–465

    Article  Google Scholar 

  39. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trend Ecol Evol 25(6):345–353

    Article  Google Scholar 

  40. Renkonen O (1938) Statistisch-ökologische Untersuchungen über die terrestische Käferwelt der finnischen Bruchmoore. An Zool Soc Zool-Bot 6:1–226

    Google Scholar 

  41. Richards KW (1993) Non–Apis bees as crop pollinators. Revue Suisse Zool 100:807–822

    Article  Google Scholar 

  42. Sadler JP, Small EC, Fiszpan H, Telfer MG, Niemela J (2006) Investigating environmental variation and landscape characteristics of an urban–rural gradient using woodland carabid assemblages. J Biogeogr 33:1126–1138

    Article  Google Scholar 

  43. Salisbury A, Armitage J, Bostock H, Perry J, Tatchell M, Thompson K (2015) Enhancing gardens as habitats for flower-visiting aerial insects (pollinators): should we plant native or exotic species? J Appl Ecol 52:1156–1164

    CAS  Article  Google Scholar 

  44. Shannon CE, Weaver W (1963) The mathematical theory of communication. University of Illinois Press, Urbana

    Google Scholar 

  45. Sikora A, Kelm M (2012) Flower preferences of the Wrocław botanical garden bumblebees (Bombus spp.) J Apic Sci 56(2):27–36

    Google Scholar 

  46. Sikora A, Michołap P, Kelm M (2016) Flowering plants preferred by bumblebees (Bombus Latr.) in the botanical garden of medicinal plants in Wrocław. J Apic Sci 60(2):59–67

    CAS  Google Scholar 

  47. Sørensen T (1948) A method of establishing groups of equal amplitude in plant sociology based on similarity of species and its application to analyses of the vegetation on Danish commons. Kongelige Danske Videnskabernes Selskab 5(4):1–34

    Google Scholar 

  48. Steffan-Dewenter I, Munzenberg U, Burger C, Thies C, Tscharntke T (2002) Scale–dependent effects of landscape context on three pollinator guilds. Ecology 83:1421–1432

    Article  Google Scholar 

  49. Sutcliffe GH, Plowright RC (1988) The effects of food supply on adult size in the bumblebee Bombus terricola Kirby (Hymenoptera: Apidae). Canad Entomol 120:1051–1058

    Article  Google Scholar 

  50. Widmer A, Schmid-Hempel P (1999) The population genetic structure of a large temperate pollinator species, Bombus Pascuorum (Scopoli) (Hymenoptera: Apidae). Molec Ecol 8:387–398

    CAS  Article  Google Scholar 

  51. Wood TJ, Holland JM, Goulson D (2015) A comparison of techniques for assessing farmland bumblebee populations. Oecologia 177:1093–1102

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

We acknowledge Prof. Tadeusz Pawlikowski (Toruń, PL) for his helpful comments on earlier versions of this manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Paweł Michołap.

Additional information

Paweł Michołap and Aneta Sikora are Co-first author

Rights and permissions

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Michołap, P., Sikora, A., Kelm, M. et al. Variability of bumblebee communities (Apidae, Bombini) in urban green areas. Urban Ecosyst 20, 1339–1345 (2017). https://doi.org/10.1007/s11252-017-0686-x

Download citation

Keywords

  • Bumblebees
  • Urban biodiversity
  • Green space
  • Area