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Download Full-Text DOI: 10.2478/jas-2014-0003 J. APIC. SCI. Vol. 58 No. 1 2014J. APIC. SCI. Vol. 58 No. 1 2014 Original Article Bees (Hymenoptera, apoidea, apiformes) in tHe agricultural landscape of Bulgaria: species diversity Józef Banaszak1* Bojana Dochkova2 1Institute of Environmental Biology, Kazimierz Wielki University, 12 Ossolińskich Av., 85-093 Bydgoszcz, Poland 25800 Pleven, 23 San Stefano, ap. 4, Bulgaria *corresponding author: [email protected] Received 27 December 2012; accepted 15 January 2014 a b s t r a c t Wild bees (apiformes) were studied in 4 crop fields and 8 refuge habitats for 2 - 5 years in agricultural landscapes in the pleven and plovdiv regions of Bulgaria. in total, 233 bee species were recorded. Bee forage plants visited by the honey bee and wild apiformes are listed for each refuge habitat. species composition is given for individual habitats, including fields of alfalfa m( edicago sativa), oilseed rape (Brassica napus), sunflower (Helianthus annuus), and radish (raphanus sativus). species richness and dominance structure of bee communities in the 2 regions are compared, and species responsible for significant differences are identified. Keywords: Bulgaria, dominance structure, Hymenoptera: apoidea: apiformes, pleven region, plovdiv region, species diversity. introduction pollination and pollinators from north-eastern Bulgaria (Ruse) were also investigated by Dimitrov Although Bulgaria lies at the borders of several (1984, 1987, 1990, 1992a, b), Dimitrov et al. (1987), zoogeographic regions, the Bulgarian fauna of and Dimitrov and Dimitrova (1991a, b). Dimitrov et al. Hymenoptera, including wild bees (Apiformes), is (1992) additionally studied pollinators of sunflower poorly studied. Among the Apiformes, bumblebees in the Ruse region. In the available literature, there is are relatively well known, mostly thanks to Pittioni’s no information on the total number of bee species in (1938, 1939) research on Bulgaria and the whole Bulgaria, but the number is certainly high. Thus, the Balkan Peninsula, supplemented by Atanassov published literature currently includes only scanty (1939, 1974). Other wild bees have been investi- reports on the bee fauna of this country. gated mostly by the latter author, e.g., Halictidae Here we present data on wild bees collected in (Atanassov, 1960) and Xylocopa (Atanassov, 2 types of agricultural landscapes: in the Danubian 1962a), who also published faunistic lists for the Plain (Pleven region in northern Bulgaria) and in Balkan Mountains (Stara Planina) and the Petrič the Upper Thracian Plain (Plovdiv region in central region (Atanassov, 1962b), and from the island of Bulgaria). Material was collected in 1986 - 1991, Tasos (Atanassov, 1965). In the 1970s and ‘80s, mostly along field margins and within fields of more attention was paid to pollinators of crop plants, selected crop plants. especially alfalfa, and to yields of this valuable forage The study aims were (1) to assess the diversity plant as well as human management of Megachile and abundance of Apiformes in these 2 types of rotundata F. (= M. pacifica Panz.) for pollination of agricultural landscapes and (2) to investigate the alfalfa seed production fields. Most information on dominance structure of pollinating insects and their this subject can be found in numerous publications phenology in these regions. by Dochkova and colleagues concerning the Pleven region (e.g., Dochkova, 1981a, b, 1982a, b, 1984; Dochkova et al., 1981a, b, c, d, 1984, 1987). Alfalfa Unauthenticated 29 Download Date | 2/9/16 10:27 AM Banaszak and Dochkova Bees of Bulgaria: species diversity material and metHods to ANOSIM and ADONIS) may be used to indicate dif- ferences between groups of objects in multidimen- Field research was conducted from April/May to sional space (Dufrêne and Legendre, 1997; Hannon September/October in 1986 - 1991, but the number and Sisk, 2009). of years varied between regions and individual study To identify which species in the community are sites, as explained in the list of study sites below. In responsible for the lack of homogeneity between the first year, research was initiated in late July. groups of samples, we calculated indicator values The insects were caught with an aerial insect net (IndVal) of bee species recorded in those areas by searching on flowers and in favorite bee nesting (Dufrěne and Legendre, 1997). The IndVal is based sites. Bee abundance was assessed once or twice a on within-species abundance and occurrence com- month using the transect method (Banaszak, 1980), parisons in specified group. In addition, the IndVal which consists of walking along a linear transect method makes it possible to evaluate the strength (200 m long, 1 m wide) and counting or, if necessary, of association between a given species and a given catching observed insects. The investigations were habitat. For this reason, IndVals were calculated conducted in conditions favorable for bee activity, i.e., for the whole collected material. If an IndVal was when air temperature was ≥20ºC and the wind was higher than 0.24, then the species was classified not strong. Obviously, we did not catch the species as strongly associated with the given habitat. The that could be readily identified, such as the honey significance of IndVals was confirmed by a randomi- bee and some of the larger wild bees. Each sample zation procedure with 1000 replications. The above was composed of insects noted or caught in an area analyses were performed in the R software envi- of 200 m2. Bee abundance was next calculated and ronment (R Development Core Team, 2008) with expressed as number of individuals per hectare. the use of vegan (Oksanen et al., 2011) and labdsv On every sampling occasion, 2 such samples were libraries (Roberts, 2010). collected at each site. In further analysis, those To compare species diversity between the landscapes coupled transects are considered as one sample. and between individual sites, we used species ac- While counting the insects, we also recorded species cumulation curves, which are analytical estimates of visited bee forage plants. As a result, a list of bee (using the MaoTau estimator) of the expected forage plants was compiled for individual sites. number of species for the given number of samples To identify differences in the structure of wild bee (Gotelli and Colwell, 2001). As Gotelli and Colwell communities between the study sites located in two (2010) observed, lack of independence between agro-ecological landscapes (Pleven and Plovdiv), we samples can be neglected if rarefaction curves are used non-metric multidimensional scaling (NMDS). functions of the number of samples. Comparison of Similarity between samples was assessed on the species richness with unequal sampling effort, which basis of Bray-Curtis distances because of their close incorporates sample-based rarefaction curves, is association with changes in community composi- often used (Calvillo et al., 2010; Banaszak-Cibicka tion (Faith et al., 1987). Ordination was used for the and Żmihorski, 2012; Żmihorski et al., 2013). samples where at least 5 individuals were observed, To estimate the true species number, we applied and the variables were the species represented by 2 estimators: Chao2 (Chao, 1984) and Jackknife2 at least 5 individuals. The results reflected major (Burnham and Overton, 1979). Chao2 is a simple * patterns in the communities. Statistical signifi- estimator of the true species number (S chao2) in cance of differences between communities (groups the community, based on the number of observed of samples) was assessed using a multi-response species (Sobs) and rare species in the collected permutation procedure (MRPP). This method tests material, i.e., those present in a single sample (a) or a hypothesis that there are no differences in species in 2 samples (b): composition between study sites (Zimmerman a2 S* = S + ( ) et al., 1985; Bonner et al., 2009) and is based on the chao2 obs 2b matrix of Bray-Curtis distances to compare mean dissimilarity within groups to dissimilarity between The estimator is the lower limit of the estimation and groups. The method estimates not only statistical serves well for data sets where most information is significance but also the A statistic and is a measure concentrated in low-frequency classes, i.e., where of within-group homogeneity compared to random a majority of species are rare. First- and second-or- homogeneity. Its value varies from 0 (random) to der jackknife estimators are methods for reducing 1 (all elements identical in the group). MRPP (similar estimation error. Second-order jackknife estimates 30 Unauthenticated Download Date | 2/9/16 10:27 AM J. APIC. SCI. Vol. 58 No. 1 2014 the true species number on the basis of the number Mean annual precipitation is 580 - 600 mm, and of species present in a single sample (uniques, L) and monthly precipitation is highest in May - June. Snow in 2 samples (duplicates, M): cover lasts about 48 days. Autumn frost starts on October 17 - 21, and late spring frost is recorded L(2n-3) M(n-2)2 until April 6 - 10. In the northern part of the region, Sjack = Sobs + [ - ] n n(n-1) carbonate chernozems are most common, while in Individual-based rarefaction curves and expected the south, typical chernozems and grey forest soils species richness were calculated using Estimate prevail. Alluvial soils are found in river valleys. Land S software (Colwell, 2006). relief is varied. Most of the area is covered by arable To compare bee dominance structure between fields (79.3%) and managed meadows (9.9%), and crop fields and semi-natural habitats, we used the the crop plants cultivated there include wheat, barley, maize, sugar beet, tobacco, sunflower, alfalfa, evenness index (EQ), which is not correlated with species number (S) (Smith and Wilson, 1996), as well grape vines, and fruit trees. as the slope angle of rank-abundance curves for In 1990 - 1992, field research was conducted in most frequent species (top 40%) in the community.
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