Variability of Bumblebee Communities (Apidae, Bombini) in Urban Green Areas

Urban Ecosyst DOI 10.1007/s11252-017-0686-x

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

Paweł Michołap1,2 & Aneta Sikora2 & Maria Kelm1 & Marcin Sikora2

# The Author(s) 2017. This article is an open access publication

Abstract Based on current research the agglomerations are created in a size of at least 30 ha. Such sites provide conditions potentially desirable habitats for bumblebees. However, the for the most diversified bumblebee species communities. Sites relationship between the biodiversity of these bees and the smaller than 30 ha can play an important role as refuges, and green areas where they live is poorly understood. The aim of allow migration to all pollinators. the study was to estimate the influence of green areas (ranging from 8 to 102 ha) of big cities on bumblebee species richness, Keywords Bumblebees . Urban biodiversity . Green space . composition, and the relative number of these insects. The Area 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 Introduction shrubs. Species richness and abundance of bumblebees was determined by direct observation during 30 min. The gathered Both in Poland and in other European countries, there has been a materials were used to calculate how areas of urban green continuous decline in bumblebees and their habitats, starting from space affected qualitative and quantitative bumblebee com- the 1980s. The main reasons for this are: the loss and fragmen- munity structure. In total, 13 species of bumblebees tation of habitats, pesticide usage,disease,parasites, non-native (Bombus Latr.) were recorded, of which 3 belonged to cuckoo species, climate change, and the interaction between these factors. bumblebees (Psithyrus subgenus). The share of the most sim- This situation could cause serious disruptions in the functioning ilar groups was congregated in green areas not smaller than of nature, and economic losses as bees are important pollinators. 30 ha. This was proved by analysis of qualitative structure It is estimated that 35% of the world’sfoodsupplyentirelyde- (Sørensen index), quantitative structure (Renkonen index), pends on these insects (Klein et al. 2007; Potts et al. 2010). and qualitative-quantitative structure (Cody’s index). The Bumblebees are particularly important pollinators in green- number of bumblebee species in the surveyed green areas houses, e.g. tomatoes. They are also specialized, unlike some (r = 0.7497) was decisive for the arrangement of the mutual other bee species, in causing the flower to vibrate – the phenom- similarity of group structure. Green urban areas should be enon known as buzz pollination. Moreover, a large number of plant species are mainly or exclusively pollinated by bumble- Paweł Michołap and Aneta Sikora are Co-first author bees. This generates a strong relationship between the survival of plant species and bumblebees’ presence (Corbet et al. 1991). * Paweł Michołap At a moment when a particular insect Bvanishes^ from the hab- [email protected] itat occupied by a plant community the Bdomino effect^ starts, which impacts herbivores and other dependent animal species 1 The Faculty of Life Sciences and Technology, Department of Plant (Corbetetal.1991; Goulson 2010;Goulsonetal.2005; Protection, Wrocław University of Environmental and Life Sciences, Pawlikowskietal.2016). pl. Grunwaldzki 24a, 53-363 Wrocław, Poland In the face of the decreasing amount of agricultural areas 2 Natura i Człowiek Association, ul. Legnicka 65, suitable for bumblebees, the urban environment is gaining grow- 54-206 Wrocław, Poland ing interest in the context of their active protection (Goddard Urban Ecosyst et al. 2010). The attractiveness of urban green areas for sustain- Materials and methods ing diverse resources for bumblebees was recorded in parks in San Francisco (McFrederick and LeBuhn 2005) and suburban The study was conducted in 2011 and 2012 on 12 sites of areas in Great Britain (Goulson et al. 2002; Osborne et al. 2008). Wrocław (Poland) green areas. These areas, ranging from 8 Cities, from the ecological point of view, are a unique mo- to 102 ha, were parks, cemeteries, railways and wasteland saic of habitats with residential, commercial, industrial and (Fig. 1). Habitats in each surveyed area were mainly formed infrastructure character, among which there are green areas by trees and shrubs. (Breuste et al. 2008). The green areas of a city are very di- Species richness and abundance of bumblebees were deter- verse, and apart of man-made gardens or parks, there are also mined by direct observation during 30 min (= sample). enclaves of natural and semi-natural plant communities Observations were conducted once per month between March (Chudzicka et al. 1998) with characteristic sets of plant and and September, from 10:00 am to 5:00 pm, in favourable weath- animal species (Niemela 1999). The essential condition for the er conditions for bee flights (Pawlikowski 2010). Bumblebees bumblebees’ occurrence, regardless of the habitat type, is the were counted on visited plant species. Specimens of Bombus availability of food sources (Alford 1975). Therefore, a special terrestris and Bombus lucorum were counted together, as it is role in urban areas is attributed to such green areas, which hard to distinguish between them during field surveys. accumulate vast numbers of flowering plants. The primary, Individual specimens of workers and males castes, impossible but not the only factor which affects the abundance of bum- to identify in the field, were caught and euthanized with ethyl blebees, is flora richness (Widmer and Schmid-Hempel 1999; acetate (method approved by the Regional and General Director Steffan-Dewenter et al. 2002; Diaz-Ferero et al. 2012; Sikora of Environmental Protection in Poland for 2011–2012). The and Kelm 2012; Sikora et al. 2016). It also turns out that not specimens are stored in the Department of Plant Protection, only do habitat characteristics have an impact on bumblebees the University of Life Sciences, Wrocław. biodiversity, but also factors in the spatial landscape scale, The gathered materials were used to identify the structure of such as the areas which surround particular habitats bumblebee communities on the study sites. The structure of (Hatfield and LeBuhn 2007). In the mosaic environment of a distanced communities was described using the number of big city the attractiveness of green spaces should also be de- species (S), average density (At), an index of total species termined by their areas. So far, this relationship has not been diversity (H′), and an evenness index (J’). Average density strictly defined (Hatfield and LeBuhn 2007; Bates et al. 2011). (At) was the number of recorded specimens on the site per The aim of the study was to estimate the influence of the 30 min of observation. The Shannon and Weaver (1963)was green spaces of big cities on bumblebee species richness, used as a formula to calculate the index of general species composition, and the relative number of bumblebee commu- diversity. The evenness index of species frequency distribution nities in Wrocław. was calculated using Pielou (1966). The qualitative similarity

Fig. 1 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 Urban Ecosyst of the distanced communities (QS) was calculated using the (Psithyrus subgenus) (Table 1). In Szczytnicki Park (P1) the Sørensen (1948), while quantitative similarity (Re) was deter- highest number of bumblebee species (12) was observed, mined by using the Renkonen (1938). Cody (1970)wasused whereas the lowest species number (5) was recorded on for quantitative and qualitative comparisons of bumblebee Gajowe Wasteland (W2) and Żernicka Railway (R2). communities. The QS and Re indices were selected in order The highest average density of bumblebees (At) was re- to assess the similarity of the communities according to their corded in the Gajowe Wasteland area (W2) – 68.5 speci- adequate representation of species number and density in the mens/30′, while the lowest occurred in the Zachodni Park area communities along an appointed gradient of the surveyed (P3) – 13.42 specimens/30′. areas’ size. The qualitative and quantitative similarity of habi- On the qualitative diagram (Fig. 2), based on the Sørensen tats was calculated using the MS EXEL program, and the index of species similarity (QS), 7 communities with predom- graphic file was generated in PHOTOSHOP CS6 software. inant mutual similarity above 77% were distanced. Those

Specific structure parameters (S, At,H′,J’) were additionally communities were present on the surveyed sites above surveyed in terms of the relationship with the size of the hab- 30 ha. The other 5 communities, within smaller areas P2, itats. Structure parameters were calculated according to corre- R2, R1, W1 and W2, showed lower mutual similarity. lation analysis, with a significance level of p ≤ 0.05. Amongst them, the smallest similarity to the others (less than Calculations were made with STATISTICA v 6.0 software. In 50%) was characteristic for the community in area R2. order to define the surveyed site areas the Wrocław Map of On the quantitative diagram (Fig. 2), based on the Renkonen Geographic Information System was used, together with mea- index (Re), 7 communities with area above 30 ha have been suring applications available at: www.geoportal.wroclaw.pl. 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- Results quantitative Cody’s index (Fig. 3), bumblebee communities clearly concentrate in regard to P6 and C2 communities. In the 12 surveyed habitats 14 species of bumblebees (Bombus Within the range of average T value there are 7 communities Latr.) were recorded, in which 3 belong to cuckoo bumblebees from the sites of 30 ha area each.

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

Site* n Bombus sp.** N At H′ J’

Area [ha] boh hor hum hyp lap pas pra rdr rup syl ter ves vet

P1 103 12 ni 2 9 1 1 124 75 3 1 30 1 174 26 447 37.25 0.68 0.63 %N 0.5 2.0 0.2 0.2 27.7 16.8 0.7 0.2 6.7 0.2 38.9 5.8 P3 72 12 ni 4 2 52 37 4 1 9 51 1 161 13.42 0.45 0.47 %N 2.5 1.2 32.3 23.0 2.5 0.6 5.6 31.7 0.6 P4 60 12 ni 155 1798951 2528013 35129.250.750.75 %N 4.3 1.4 4.8 27.9 27.1 0.3 7.1 0.6 22.8 3.7 C2 53 11 ni 1 16 29 63 1 2 76 8 196 17.82 0.63 0.70 %N 0.5 8.2 14.8 32.1 0.5 1.0 38.8 4.1 P6 35 11 ni 2 6 3 10 144 4 9 3 340 28 549 49.91 0.48 0.48 %N 0.4 1.1 0.6 1.8 26.2 0.7 1.6 0.6 61.9 5.1 C1 30 11 ni 10 6 2 28 35 7 15 1 80 25 209 19 0.79 0.79 %N 4.8 2.9 1.0 13.4 16.8 3.4 7.2 0.5 38.3 12.0 P5 30 12 ni 2 3 71 46 2 2 34 159 12 331 27.58 0.63 0.66 %N 0.6 0.9 21.5 13.9 0.6 0.6 10.3 48 3.6 P2 26 12 ni 20 2 61 128 3 2 52 2 270 22.5 0.59 0.65 %N 7.4 0.7 22.6 47.4 1.1 0.7 19.3 0.7 R2 22 10 ni 144 71 16 54 4 289 28.5 0.53 0.76 %N 49.8 24.6 5.5 18.7 1.4 R1 16 10 ni 1 2 108 29 2 7 53 1 203 20.3 0.53 0.59 %N 0.5 1.0 53.2 14.3 1.0 3.5 26.1 0.5 W1 8 10 ni 2 1 215 42 113 1 374 37.4 0.43 0.55 %N 0.5 0.3 57.5 11.2 30.2 0.3 W2 8 10 ni 481 80 2 5 117 685 68.5 0.37 0.53 %N 70.2 11.7 0.3 0.7 17.1

*Sites according to Fig. 1 **Bumblebee species: boh – Bombus bohemicus,hor– B. hortorum,hum– B. humilis,hyp– B. hypnorum,lap– B. lapidarius,pas– B. pascuorum,pra– B. pratorum,rdr– B. ruderarius,rup– B. rupestris,syl– B. sylvarum,ter– B. terrestris and B. lucorum,ves– B. vestalis,vet– B. veteranus n number of samples, ni number of specimens, %N domination, N total number of specimentsl, At average density, H′ diversity (Shannon and Weaver 1963), J’ evenness (Pielou 1966) Urban Ecosyst

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).

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 annu- lar-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 Fig. 2 Diagrams of qualitative similarity (QS) and quantitative similarity (Re) of bumblebee communities according to the gradient of green areas (MacArthur and Wilson 1967). The theory states that the bigger in Wrocław 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)livingin 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 Fig. 3 Dendrite resemblance presenting species diversity of bumblebee communities in green areas of Wrocław. The communities refer to the influencing the bumblebees abundance and their species di- circle of Cody’s index average values (T) versity (Widmer and Schmid-Hempel 1999;Steffan- Urban Ecosyst

Fig. 4 Structure parameters of bumblebee communities according to the gradient of green areas in Wrocław

Dewenter et al. 2002; Diaz-Ferero et al. 2012;Pardeand confirm the principle that a few but adequately selected plant Philipott 2014; Salisbury et al. 2015;Woodetal.2015). species as food sources might provide suitable conditions for However, on the Wrocław study sites the number of visited the development of numerous bumblebee families. This has flowering plants did not correlate with the size of the site significant importance in rural environments, where the eco- r = 0.0792 (Fig. 5). Therefore, the quality factors like the nomic use of bumblebees is mainly focused on plant mono- degree of food attractiveness and abundance in the habitat cultures (Goulson 2010). seem to be more important than the number of flowering Isolation in extremely fragmented city habitats is a serious plants. The bumblebees abundance depends primarily on the threat for bumblebee families. Smaller populations are more quality, availability and stability of food sources in the vulnerable to extinction due to environmental changes inhabited area. Comparing the bumblebees’ density in urban (Frankham et al. 2002). It was confirmed that populations which parks, cemeteries and allotments, the highest value was pre- cannot freely move between habitats are forced to inbreed, and sented in species-rich flower gardens (Ahrne 2008). In such this leads to a decrease in the condition of the whole population places, with a high diversity of flowering plants, bumblebee (Krebs 2009). Habitat fragmentation may cause a situation density can reach 8 specimens per 100 m2 (Matteson and where too small sites with food plants will not be attractive for Langellotto 2009), while on cultivated fields in England only some bumblebee species (Mayer et al. 2012). 4–5 specimens per 100 sq. m (Carvell et al. 2004) and less Within the city space the sequences of green areas along than 1 specimen on 100 sq. m on meadow habitats in Sweden roads should allow migration. In the Wrocław agglomeration (Öckinger and Smith 2007). Observed trophic interactions such a function can be fulfilled by railway sites with attractive

Fig. 5 Relationship between the number of visited flowering plants (P) and the size of green areas in Wrocław Urban Ecosyst ruderal plants. Plants from the Fabaceae family could be a Acknowledgements We acknowledge Prof. Tadeusz Pawlikowski ń perfect pollen source for visiting bumblebees (Goulson and (Toru , PL) for his helpful comments on earlier versions of this manuscript. Darvill 2004). The value of these sites is undoubtedly in- Open Access This article is distributed under the terms of the Creative creased by the presence of one of the rarest and endangered Commons Attribution 4.0 International License (http:// bumblebee species in Poland – Bombus veteranus. creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appro- International efforts to preserve the environment are focused priate credit to the original author(s) and the source, provide a link to the mainly on large ecosystems, usually very little altered by hu- Creative Commons license, and indicate if changes were made. man 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 References important for the quality of life in a more urbanised society (Chiesura 2004). 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