DOI: 10.2478/v10289-012-0027-5 Vol. 56 No. 2 2012 Journal of Apicultural Science 89

SPATIAL DIVERSIFICATION OF BEE (: APOIDEA: APIFORMES) ASSEMBLAGES IN FOREST COMMUNITIES OF THE SUCHEDNIÓW-OBLĘGOREK LANDSCAPE PARK

Jolanta Bąk-Badowska

Institute of Biology, Jan Kochanowski University, ul. Świętokrzyska 15, 25-406 Kielce, Poland. e-mail: [email protected] Received 01 August 2012; accepted 29 October 2012

Summary The aim of the study, carried out from April to October in 2004 and 2005, was to characterise bee (Apiformes) assemblages in the phytosociologically diversifi ed forest communities of the Suchedniów-Oblęgorek Landscape Park. Moericke colour traps were used to capture the bees. The fi ve study sites yielded 76 bee species. There was a predominance of representatives from the families Apidae (28 species, 900 individuals) and (20 species, 222 individuals). The indices of species diversity (H’) and evenness (J’) reached their highest values in a mixed coniferous forest (BM) site, and reached their lowest values in a fi r forest (BJ) site. Qualitative and quantitative similarity of assemblage structure was highest in assemblages in mixed coniferous forest, mesic coniferous forest, and oak-hornbeam forest habitats, decreasing in fl oristically poor habitats not favourable to nesting, i.e. fi r forest and riparian forest. Traps placed on the forest fl oor in ground cover contained more individuals and species of bees, with 1192 individuals (88.8%) and 76 species, than in the canopy layer, with 150 individuals (11.2%) and 23 species. This trend was consistent across all the habitats in the Landscape Park. Keywords: Apiformes, assemblage structure, forest habitats, vertical distribution, Suchedniów-Oblęgorek Landscape Park. INTRODUCTION 1987, 1990; Banaszak and Cierzniak, Bees have been relatively well studied 1994; Krzysztofiak, 2001; Cierzniak, in Poland, with most research focusing 2003; Banaszak and Jaroszewicz, on open areas such as meadows, fields, 2009; Tuell and Isaacs, 2009). and xerothermal grasslands, which are Bees’ natural resources depend on several populated by particularly abundant factors, both natural and anthropogenic, bee assemblages (Dylewska and including habitat type, moisture levels Noskiewicz, 1963; Dylewska, and fertility, and the resulting diversity 1966; Banaszak and Plewka, 1981; of plant communities. Research by Pawlikowski, 1985; Oertli et al., 2005). Pawlikowski (1992) and Krzysztofiak Forest areas were formerly believed to not (2001) showed that the species richness be very attractive to bees. It was only in the and diversity of bees in the forest decrease early 1980’s that interest in the presence as the forest stand grows older. There are of bees in forests began to grow. Existing also changes in habitat conditions. These studies have taken into account not only changes are mostly owing to decreased those species associated with plants availability of food plants and nesting sites found on the forest floor in ground cover, as individual layers of forest vegetation but also those captured in tree canopies contribute to a habitat’s microclimate. The (Pawlikowski, 1985, 1990; Banaszak, amplitude of changes in temperature and moisture levels are reduced. 90

One effective way to preserve the The dominant type of soil is podzolic soil biological diversity of , including with a shallow humus horizon. This soil is bees, is to protect species in their natural mostly found on the slopes of hummocks habitats. Accordingly, studies of areas and in river floodplains. The soil is stony that have suffered the least anthropogenic and considerably acidified. impact, such as national parks, nature The greatest natural asset of the Park reserves and landscape parks are is its forests, which occupy nearly 90% particularly valuable. of its area. These forests are what has Despite many years of research on remained of a large and mostly natural the structure of bee assemblages in the forest complex called Holy Cross Primeval Małopolska Upland, data on this Forest. The dominant forest type is a fertile group are still incomplete. As part of mixed coniferous forest, with smaller investigations of bees of protected areas areas supporting oak-hornbeam forests, within the Upland, a study was conducted ash-aspen riparian forests, swamp forest, to characterise bee assemblages in and the Carpathian beechwood. The most phytosociologically diversified forest important forest-forming tree species are communities of the Suchedniów-Oblęgorek pine (52%) and fir (31%). Landscape Park (S-OLP). An earlier study Study sites were set up in the Park in from 1999-2000, carried out in three types a variety of forest habitat types. They are of phytocoenosis in the Park, was only presented in Fig. 1 against the UTM square concerned with the Bombus species (Bąk, grid (Enghoff and Nielsen, 1978). 2003). Site 1, UTM: DB75; Zagnańsk Forest Area of study Inspectorate, Bartków forest district, Suchedniów-Oblęgorek Landscape division 77 Park is located in the Małopolska Upland This site is made up of a mixed coniferous in the macroregion of the Kielce Upland forest (BM) (Querco roboris-Pinetum). (Kondracki, 2002) to the north of the The stand is 60-70 years old. The tallest town of Kielce. The Świętokrzyski (Holy layer of trees is made up of Quercus robur Cross) National Park is the border in the and Pinus sylvestris. Under the tallest north-west. It is the largest landscape park layer there is a sub-canopy layer, formed in the Małopolska Upland, covering an area mainly of Pinus sylvestris, Quercus robur of 21 407 ha (Fig. 1). The park consists and Carpinus betulus. The shrub layer has of two separate areas surrounded by one a of 30% density. This layer is dominated protection zone with an area of 25 681 ha. by Quercus robur, Frangula alnus and The eastern part, known as the Suchedniów Corylus avellana. The herb layer is not area, is covered with mixed forests and dense (50%) and is strongly shaded, with embraces the Suchedniów Plateau and Vaccinium myrtillus, Anemone nemorosa, the Kołomań Hills. The western park, the Convallaria majalis, Melampyrum Oblęgorek area, includes the Oblęgorek nemorosum, Hieracium sp. and others. Range of the Holy Cross Mountains. A total of 48 species of vascular plants The entire area of the Park is part of were found at this site. a climatic unit called Holy Cross Upland Site 2, UTM: DB75; Suchedniów Forest by Romer (1949). The climatic conditions Inspectorate, Wilczy Bór forest district, here change with altitude above sea level. division 100 Mean annual ambient air temperature in This is the site of the mesic coniferous the Park does not vary much, ranging from forest (BS) (Leucobryo-Pinetum). The 6.8oC to 7.6oC. The highest precipitation forest stand is 60 years old and has is in June (100 mm), July (99 mm), and a density of 60%, with a predominance of August (73 mm), with a mean annual Pinus sylvestris and Betula pendula. The total precipitation between 600 mm and understorey is 10%, consisting mainly of 770 mm. Quercus robur, and more rarely Sorbus Vol. 56 No. 2 2012 Journal of Apicultural Science 91 Fig. 1. Location of study sites in Suchedniów-Obl as in Tab.1), b - Park boundary, c - protection zone boundary, d - roads, e rivers, f forests, g UTM grid ę gorek Landscape Park plotted against the UTM grid: a - study sites (numbered 92 aucuparia, Pinus sylvestris and Betula Site 5, UTM: DB75; Zagnańsk Forest pendula. The herb layer is of 70% density. Inspectorate, Bartków forest district, It is made up of Vaccinium myrtillus, division 119 Vaccinium vitis-idaea, Melampyrum This is the site of the riparian forest pratense, Calluna vulgaris, Carex pilulifera complex (LG) (Fraxino-Alnetum) and others. The number of vascular plant on humic, very moist soils. The forest species identified was 39. stand is approx. 50 years old and is made Site 3, UTM: DB85; Suchedniów Forest up of Alnus glutinosa. The understorey Inspectorate, Osieczno forest district, has a 40% density, with a predominance division 107 of Alnus glutinosa and Corylus avellana. This is the site is of the oak-hornbeam The herb layer, of 90% density, consists forest (GR) (Tilio cordatae-Carpinetum of hygrophilous and umbrophilous species, betuli). The forest stand is approximately such as Filipendula ulmaria, Crepis 60 years old. The tallest layer of trees paludosa, Lycopus europaeus, Galium have a 70% density. The tallest layer is palustre, Peucedanum palustre and others. mostly made up of Quercus robur, Betula A total of 26 species of vascular plants pendula, Tilia cordata, Carpinus betulus were identified within this site. and Populus tremula. A sub-canopy layer is formed of Quercus robur, Carpinus MATERIAL AND METHODS betulus and Fagus sylvatica with a small Bee assemblages of selected sites in the admixture of Abies alba. The understory Suchedniów-Oblęgorek Landscape Park is dominated by Carpinus betulus, Abies were studied from April to October in alba and Corylus avellana. The shrub 2004 and 2005. Bees were collected from layer density reaches 40%. The herb layer, Moericke colour traps (Moericke, of low density and heavy shading, consists 1951). The capture data were used to study of Anemone nemorosa, Galeobdolon the vertical distribution of the insects in luteum, Hepatica nobilis, Dentaria different forest habitats. The colour trap bulbifera, Viola reichenbachiana, method also provides data on the species Pulmonaria obscura, Rubus hirtus and composition of bee assemblages and the others. A total of 32 species of vascular patterns of the appearance of individual plants were identified. species. Site 4, UTM: DB75; Suchedniów Forest The Moericke colour traps used in this Inspectorate, Św. Góra forest district, study were white plastic vessels, 20 cm in division 96 diameter and 15 cm deep, half-filled with This is the site of the fir forest (BJ) a liquid composed of 95% water, 4.8% (Abietetum polonicum). The tree ethylene glycol and 0.2% surfactant. Three community is 70 years old, shady, with traps were placed on each site in two layers a five-layer structure. In the tree and shrub of forest: in the ground cover layer on the layer, the dominant species is Abies alba. ground, and in tree canopies at a height of Another species in the tree layer is Fagus 10-12 m. Insects captured were removed sylvatica. This species has a 80% density. and the liquid replaced at two-week A sub-canopy layer of 40% density, is intervals. made up of Fagus sylvatica, Abies alba Insects collected over 14 days and Carpinus betulus. The understory represented one sample. All samples were has a similar density and consists mainly used to determine the structure of the bee of Abies alba and Carpinus betulus, with assemblages. A bee assemblage is defined a smaller contribution of Sorbus aucuparia. here as a group of species co-existing in The herb layer consists of: Maianthemum a given area. It consists of species that bifolium, Oxalis acetosella, Luzula pilosa nest in the area and those which fly in and Vaccinium myrtillus. The number of from adjacent areas to search for food. It vascular plant species identified was 24. was assumed that bees captured in traps Vol. 56 No. 2 2012 Journal of Apicultural Science 93 1 1.1 1.1 0.1 0.1 0.1 0.1 1.7 1.8 0.6 0.4 0.5 0.3 0.5 0.5 0.8 0.8 5.4 0.2 0.2 1 8 2 7 3 2 3 4 7 7 5 2 11 11 14 15 15 72 23 24 22 1.6 Total % Table 1. % tree LG canopies Fraxino-Alnetum cover ground % tree BJ canopies Abietetum polonicumAbietetum cover ground % tree GR betuli canopies 1.10710.83 0.781 412.21 cover gorek Landscape Park in 2004 and 2005 Tilio cordatae-CarpinetumTilio ground ę % tree BS canopies Leucobryo-Pinetum cover ground List of bee species and individuals their dominance (%) % tree BM in forest habitats of Suchedniów-Obl canopies Querco roboris-Pinetum Querco cover ground Cock. 2 0.44 (L.) 22 5.39 (Kirby) 5 1 1.31 4 0.98 1 0.44 (F.) 25 6 6.78 28 2 7.35 9 2 4.86 (Kirby) 2 0.49 1 0.78 Nyl. 8 1.75 3 0.74 2 0.88 1 0.78 (Kirby) 2 0.49 (F.) 1 0.44 Nyl. 2 0.44 2 0.88 2 1.55 1 0.83 Nyl. 3 0.66 11 4 3.68 4 1.76 1 0.78 1 0.83 Zett. 3 1 0.88 1 0.25 2 0.88 1 0.78 (Kirby) 1 1 0.49 1 0.44 (.72131231322321.65 1.32212.332 (L.)732.19321.233 (Kirby) 4 0.88 6 1.47 1 0.44 (Kirby) 4 0.98 Species F. (L.) 4 0.88 2 0.49 8 1 4.04 Perk. 2 0.88 Smith 4 0.88 1 1 0.49 1 0.44 (Müll.) 1 1 0.49 1 0.44 1 1 1.65 (Müll.) 5 1.1 8 1.96 2 0.88 A. helvola A. A. lapponica A. A. jacobi jacobi A. A. haemorrhoa A. A. hattorfiana A. A. fulva A. A. fucata A. A. denticulata A. A. clarkella A. minutula A. A. nigroaenea nigroaenea A. A. fuscipes A. Hy. confususHy. A. bicolor barbilabris Andrena cineraria A. A. nitida A. A. subopaca A. Hylaeus cardioscapusHylaeus communis Hy. Colletes cunicularius cunicularius Colletes 9 8 4 6 5 7 2 3 11 2 3 4 56 7 89 10111213141516171819 11 17 13 12 14 15 18 19 10 16 21 20 No. Community 94 1 1 0.1 0.1 0.1 0.1 0.1 0.1 1.6 0.7 0.6 0.4 0.4 0.5 0.3 0.3 0.5 0.2 0.2 0.2 0.2 4 2 3 2 3 2 7 3 1 4 5 9 4 8 7 2 6 2 13 14 22 Total % % tree LG canopies Fraxino-Alnetum 10.83 cover ground Table 1. Continued % tree BJ canopies Abietetum polonicumAbietetum cover ground % tree GR betuli canopies cover gorek Landscape Park in 2004 and 2005 Tilio cordatae-CarpinetumTilio ground ę % tree BS canopies Leucobryo-Pinetum cover ground List of bee species and individuals their dominance (%) % tree BM in forest habitats of Suchedniów-Obl canopies Querco roboris-Pinetum Querco cover ground (F.) 1 0.25 1 0.83 (L.) 1 0.22 1 0.44 (F.) 1 0.25 2 0.88 4 3.31 (Scop.) 2 0.44 3 0.74 1 0.44 Warncke8 1.8 4 0.982 0.88 8 6.61 Smith 1 0.22 1 0.78 (Thoms.) 2 0.44 2 0.49 (F.) 3 0.66 (Imh.) 3 0.74 2 2 1.76 (Schenck) 3 0.66 1 0.44 (Kirby) 3 1.32 (L.) 3 0.66 2 0.49 2 0.88 1 0.78 (F.) 3 0.66 8 1.96 3 2.33 (Scop.) 4 0.88 3 1 0.98 1 0.44 (Kirby) 2 0.44 (Schenck) 1 0.22 (Panz.) 2 0.44 (F.) 8 1.75 1 0.44 4 3.31 Species (Rossi) 1 0.44 1 0.83 (Nyl.) 3 0.66 1 0.25 (F.) 5 1.1 Panz. 1 0.44 1 0.1 H. spinulosa H. Hoplitis claviventris M. leporina M. Melitta haemorrhoidalis Melitta Macropis europaea europaea Macropis M. fulvipes M. Dasypoda hirtipes hirtipes Dasypoda Sphecodes ephippius Sphecodes L. subfasciatum L. sexstrigatum L. L. sexnotatum sexnotatum L. L. pauxillum L. morio L. L. majus L. L. calceatum L. H. tumulorum H. Lasioglossum albipes Lasioglossum H. sexcinctus H. Halictus maculatus Halictus A. varians A. A. vaga A. Panurgus calcaratus 41 31 42 37 24 27 25 32 28 26 23 29 40 43 39 35 33 38 22 36 30 34 No. Community Vol. 56 No. 2 2012 Journal of Apicultural Science 95 1 9.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 1.6 0.7 1.2 0.4 0.3 0.3 0.3 0.8 8.8 0.2 0.2 4 3 9 5 2 2 2 2 3 4 4 1 1 1 11 14 16 22 118 122 Total % % tree LG canopies Fraxino-Alnetum Table 1.Continued cover ground % tree BJ canopies Abietetum polonicumAbietetum 10.78 cover ground % tree GR betuli canopies 10.44 gorek Landscape Park in 2004 and 2005 cover Tilio cordatae-CarpinetumTilio ę ground % tree BS canopies Leucobryo-Pinetum cover ground List of bee species and individuals their dominance (%) % tree in forest habitats of Suchedniów-Obl BM canopies Querco roboris-Pinetum Querco cover ground (F.) 1 0.22 (L.) 2 0.44 (Panz.) 3 0.66 1 0.25 (.4111.91.8 2.33313.31 (L.)411.1110.49110.883 (Panz.) (Panz.) 3 1 0.98 (Kirby) 2 0.44 3 0.74 1 0.78 6 0.4 (Kirby) 1 0.22 1 1 0.49 (Scop.)3738.753027.842812.33917.55716.61 Panz. 2 0.44 L)2.3 .91.8 0.78110.83 0.49110.881 (L.)521.532 Alfk. 2 0.49 3 1.32 (L.) 5 1.1 4 0.98 2 0.88 (Pall.) 1 0.25 2 0.88 (Kirby) 2 0.88 (L.) 32 7.0 26 4 7.35 26 2 12.33 19 1 15.50 10 2 9.92 Species (Kirby) 3 0.66 1 0.25 1 0.44 1 0.78 3 2.48 lll. 2 0.44 Jur. 2 0.44 1 0.25 1 0.44 (Panz.) (L.) 8 2 2.19 3 0.74 6 1 3.08 1 1 1.65 Anthophora furcata Anthophora pascuorum B. B. lucorum B. A. plumipes A. B. lapidarius Bombus hortorum Bombus humilis B. B. hypnorum hypnorum B. jonellus B. N.moeschleri N.signata Megachile lagopoda M. ligniseca M. Ceratina cyanea flava Nomada cruciger Epeolus N. flavoguttata Epeoloides coecutiens Epeoloides Osmia fulviventris Osmia O. rufaO. Anthidiellum strigatum 51 47 61 52 57 62 49 59 63 45 48 46 53 50 55 58 56 60 44 64 54 No. Community 96 2 1 4.1 1.6 4.7 0.7 0.7 0.7 2.7 2.4 24.5 20.1 13 10 10 10 32 27 36 55 22 63 328 Total % % tree LG canopies Fraxino-Alnetum cover ground Table 1. Continued % tree BJ canopies Abietetum polonicumAbietetum cover ground % tree GR betuli canopies gorek Landscape Park in 2004 and 2005 cover Tilio cordatae-CarpinetumTilio ę ground % tree BS canopies Leucobryo-Pinetum cover ground List of bee species and individuals their dominance (%) % tree in forest habitats of Suchedniów-Obl BM canopies 20.4420.4931.3232.33 405 52 367 41 205 22 111 18 104 17 Querco roboris-Pinetum Querco cover ground (Seidl) 21 2 5.03 5 1.23 14 6.17 8 6.25 5 4.13 (Panz.) 8 1.75 12 2.94 6 2.64 1 0.78 Skor. 2 0.44 (F.) 10 2.19 4 0.98 8 6.61 Lep. 12 2.63 2 0.49 5 2.20 10 7.35 3 2.48 (Geoffr.) 10 2.19 3 2.33 L. 71 20 19.91 110 10 29.4 32 8 17.62 31 7 29.46 30 9 32.23 (Müll.) 4 0.88 6 1.47 (L.) 15 3 3.94 6 10 3.92 5 1 2.64 6 8 10.85 8 1 7.44 (L.) 6 1.31 4 0.98 (Kirby) (L.) 16 4 4.38 10 2.45 4 2 2.64 Species individuals in layer in individuals numberTotal of individuals 457 408 227 129 121 1342 B. (Psithyrus) (Psithyrus) B. barbutellus B. (Ps.) rupestris B. (Ps.) campestris B. (Ps.) bohemicus B. pratorum B. B. sylvarum B. B. terrestris B. B. (Ps.) sylvestris numberTotal of B. ruderarius B. B. semenoviellus B. B. (Ps.) vestalis mellifera Apis 74 71 75 76 70 73 72 67 65 69 68 66 No. Community Vol. 56 No. 2 2012 Journal of Apicultural Science 97

placed on the ground penetrated the part (1998) and Banaszak (2004). The of the ground cover just above the ground nomenclature of plant species was given and low-growing herbs, while bees found after Mirek et al. (2002). The specimens in the traps hung at 10-12 m above ground were determined by the author. penetrated the topmost layer of tree canopies. RESULTS The structure of each assemblage was A total of 1342 bee individuals described with the number of samples (n), representing 76 species and 6 families the number of species (S), the number of were captured in Moericke traps during individuals (N), an index of dominance the two years of the study. The dominant (D), an index of general diversity (H’) bee families in the five study sites were (Shannon and Weaver, 1963), and Apidae (69.4%) and Andrenidae (16.5%). an index of evenness (J’) (Pielou, 1966). There were few representatives of Descriptive dominance classes, after Colletidae (3.4%) and Melittidae (3.2%) Witkowski (1975), were as follows: (Tab. 1). The most abundant genera were eudominants > 10.0% of all specimens; Bombus and Andrena. An analysis of the dominants 5.1-10.0%; subdominants number of species representing individual 2.1-5.0%; recedents 1.1-2.0%; and families found that the Apidae (28 species) subrecedents ≤ 1.0% . and Andrenidae (20 species) families Qualitative comparisons of assemblages were most numerous, and Colletidae were based on the Marczewski- (4 species) and Melittidae (5 species) Steinhaus index (Marczewski and were least numerous, the two remaining Steinhaus, 1959); families being represented by 12 species MS = 100 c/a +b - c, (Halictidae) and 7 species (Megachilidae) where a is the number of species in one (Tab. 2). The dominant species were assemblage, b is the number of species in Apis mellifera (24.5%), Bombus lucorum another assemblage, and c is the number of (9.1%), B. pascuorum (8.8%) and Andrena species common to both assemblages. haemorrhoa (5.4%) (Tab. 1). Qunatitative comparisons were based on Each forest habitat supported Renkonen’s index (1938); a structurally different bee assemblage.

Re = Σ Dmin, Querco roboris-Pinetum, mixed where Dmin is the lowest value of coniferous forest (BM) minimum dominance of a species in the The bee assemblage in the study site was assemblages being compared. composed of 55 species (457 individuals) The systematic division and ordering of (Tab. 1, 3), with a predominance of bees were given after Michener (2007), representatives from the families Apidae the nomenclature of bee species was given and Andrenidae, whose individuals after Ruszkowski and Ruszkowski accounted for 82.5% of the assemblage. Table 2. Number of bee species from individual families captured into Moericke’s traps in the ground cover and canopy layer of forest habitats in S-OLP

Community BM BS GR BJ LG Total ground tree ground tree ground tree ground tree ground tree Family cover canopies cover canopies cover canopies cover canopies cover canopies Colletidae3-2-2-2-1-4 Andrenidae95156173515120 Halictidae9-61713-1-12 Melittidae4-2-2---4-5 Megachilidae412-311-117 Apidae 25 7 23 7 16 6 13 4 10 6 28 98

The highest value of the index of species (5 species, 15 individuals) bees were diversity (H’) was 4.75, and the index of numerous (Tab. 1, 2). The dominant species evenness (J’) was 0.76 (Tab. 3). in this layer were Apis mellifera (37%), Ground cover - A total of 54 species Andrena fucata (7.7%), Bombus terrestris (405 individuals) were captured in (7.7%), A. cineraria, B. pascuorum and ground cover of the mixed coniferous B. pratorum (5.8% each) (Fig. 2). The H’ forest site (Tab. 3). The family Apidae index of species diversity was 3.04, and the was most numerous in terms of both J’ index of evenness was 0.82 (Tab. 3). the number of species and individuals Leucobryo-Pinetum, mesic coniferous (25 species, 276 individuals), and was forest (BS) followed by Andrenidae (9 species, 58 Traps in this habitat yielded individuals) and Halictidae (9 species, 408 individuals belonging to 50 species 24 individuals) (Tab. 1, 2). The most (Tab. 1, 3). The patterns of dominance abundant species were Apis mellifera were similar to those observed in the mixed (17.5%), Bombus pascuorum (9.4%), coniferous forest site, with a predominance B. lucorum (7.9%) and B. bohemicus of species and individuals from the families (5.2%). The only numerous representative Apidae (23 species, 266 individuals) and of Andrenidae was Andrena haemorrhoa Andrenidae (15 species, 88 individuals) (6.2%) (Fig. 2). The H’ index reached (Tab. 1, 2). The H’ index was 4.27, and the a maximum value of 4.83 in this layer, and J’ index was 0.68 (Tab. 3). the J’ index was 0.84 (Tab. 3). Ground cover - Traps in this layer Tree canopies - There were 52 individuals yielded 50 species and 367 individuals representing 13 species captured in the tree (Tab. 3). The most abundant families were canopies (Tab. 3). There were no species Apidae (23 species, 237 individuals) and from the families Colletidae, Halictidae Andrenidae (15 species, 77 individuals) or Melittidae (Tab. 2), while Apidae (Tab. 1, 2). The dominant species included (7 species, 35 individuals) and Andrenidae Apis mellifera (30%), Bombus pascuorum Table 3. Biocoenotic indices of bee assemblages of forest habitats in S-OLP

Community n S Σ N Σ H' Σ J' Σ Querco roboris-Pinetum BM ground cover 28 54 55 405 457 4,83 4,75 0,84 0,76 tree canopies 26 13 52 3,04 0,82 Leucobryo-Pinetum BS ground cover 28 50 50 367 408 4,23 4,27 0,75 0,68 tree canopies 25 14 41 3,2 0,84 Tilio cordatae-Carpinetum betuli GR ground cover 26 47 47 205 227 4,54 4,51 0,82 0,72 tree canopies 27 11 22 3 0,87 Abietetum polonicum BJ ground cover 28 24 24 111 129 3,56 3,48 0,78 0,56 tree canopies 28 5 18 1,74 0,75 Fraxino-Alnetum LG ground cover 28 22 22 104 121 3,66 3,59 0,82 0,57 tree canopies 25 8 17 2,29 0,76 n - number of samples S - number of species N - number of individuals H' - species diversity, based on Shannon and Weaver's formula (1963) J' - evenness, based on Pielou's formula (1963) Vol. 56 No. 2 2012 Journal of Apicultural Science 99

(8.2%), and Andrena haemorrhoa (7.6%). Ground cover - There were 47 species Colletes cunicularius was also numerously (205 individuals) (Tab. 3). Besides collected in late April and early May Apis mellifera, the dominant taxa in the low- (Fig. 3). The H’ index was 4.23, and the growing herb layer were bumble bees and J’ index was 0.75 (Tab. 3). their parasites (Bombus pascuorum - 13.7%, Tree canopies - Traps in tree canopies B. lucorum - 12.7% and B. bohemicus - yielded 14 species and 41 individuals 6.8%). The remaining 43 species made (Tab. 3). The families Apidae and up 51.2% of the assemblage (Fig. 4). The Andrenidae were represented by 7 and H’ index was 4.54, and the J’ index was 6 species, respectively, while the only 0.82 (Tab. 3). Halictidae species was Lasioglossum Tree canopies - This assemblage was calceatum (Tab. 1, 2). Two species: Bombus made up of 11 species (22 individuals) pratorum and Apis mellifera, reached the (Tab. 3). Apis mellifera was a eudominant highest dominance level (24.4% each), and (D = 36.4%). Dominants were Andrena the group of dominants comprised Andrena haemorrhoa, Lasioglossum subfasciatum, subopaca and B. lucorum (9.8% each) Bombus lucorum and B. terrestris, all with (Fig. 3). The index of species diversity (H’) a dominance index of 9.1% (Fig. 4). The for the bee assemblage of tree canopies was H’ and J’ indices amounted to 3.0 and 0.87, 3.2, and the J’ index was 0.84 (Tab. 3). respectively (Tab. 3). Tilio cordatae-Carpinetum betuli, oak- Abietetum polonicum, fir forest (BJ) hornbeam forest (GR) In the fir forest, the bee assemblage was This habitat supported species from all made up of 129 individuals belonging 6 families recorded in the study area, with to 24 species (Tab. 1, 3). There were no 227 individuals belonging to 47 species species from the family Melittidae. The (Tab. 1, 3). As in the sites described above, most numerous family was the Apidae, the dominant families were Andrenidae with 13 species and 111 individuals) (Tab. (17 species, 47 individuals) and Apidae 1, 2). The values of the H’ and J’ indices (16 species, 149 individuals) (Tab. 1, 2). were the lowest compared to the other The most numerous genera were Bombus study sites, at 3.48 and 0.56, respectively and Andrena, constituting 65.6% of the (Tab. 3). assemblage. The values of the H’ and J’ Ground cover - In the low-growing indices were 4.51 and 0.72, respectively herb layer, Moericke traps yielded (Tab. 3). 111 individuals of 24 species (Tab. 3).

Ground cover Tree canopies D [%] D [%] 20 40 18 35 16 30 14

12 25

10 20

8 15 6 10 4

2 5

0 0 A B C D E Remaining A F G H B I Remaining 49 sp. 7 sp. Species 53,8% Species 30,2% Fig. 2. Dominance patterns in bee assemblages collected in the mixed coniferous forest (BM) in the Suchedniów-Oblęgorek Landscape Park; A - Apis mellifera, B - Bombus pascuorum, C - Bombus lucorum, D - Andrena haemorrhoa, E - Bombus bohemicus, F - Andrena fucata, G - Bombus terrestris, H - Andrena cineraria, I - Bombus pratorum. 100

They were mostly bumble bees and the B. pratorum and Apis mellifera). The honey bee together accounting for 84.7% abundance of bees was also low, with of the assemblage. Dominant species 18 individuals captured (Tab. 1, 2). The were Apis mellifera (28.2%), Bombus five species were classified as eudominant lucorum (17.2%), B. sylvarum (9.1%), (B. pratorum and A. mellifera) or dominant B. pascuorum (8.2%), B. bohemicus (7.3%) (A. cineraria, B. lucorum and B. pascuorum) and B. pratorum (5.5%) (Fig. 5). The index (Fig. 5). The H’ and J’ indices were at their of species diversity was 3.56, and the index lowest in this layer, amounting to 1.74 and of evenness was 0.78 (Tab. 3). 0.75, respectively (Tab. 3). Tree canopies - Catches in the canopy Fraxino-Alnetum, riparian forest (LG) layer yielded only one species from the The bee assemblage in this habitat family Andrenidae (Andrena cineraria) was made up of 22 species representing and four species from the family Apidae 6 families. A total of 121 individuals were (Bombus lucorum, B. pascuorum, captured (Tab. 1, 3). The abundance of bees

Ground cover Tree canopies D [%] D [%] 35 30

30 25

25 20

20 15 15

10 10

5 5

0 0 A B D C J Remaining I A K C Remaining 45 sp. Species 10 sp. 41,4% Species 31,6% Fig. 3. Dominance patterns in bee assemblages collected in the mesic coniferous forest (BS) in the Suchedniów- Oblęgorek Landscape Park; A - Apis mellifera, B - Bombus pascuorum, C - Bombus lucorum, D - Andrena haemorrhoa, I - Bombus pratorum, J - Colletes cunicularius, K - Andrena subopaca.

Ground cover D [%] D [%] 18 Tree canopies 40 16 35 14 30 12

10 25

8 20

6 15

4 10

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0 0 A B C E Remaining A D L C G Remaining 43 sp. 6 sp. 27,2% Species 51,2% Species Fig. 4. Dominance patterns in bee assemblages collected in the oak-hornbeam forest (GR) in the Suchedniów- Oblęgorek Landscape Park; A - Apis mellifera, B - Bombus pascuorum, C - Bombus lucorum, D - Andrena haemorrhoa, E - Bombus bohemicus, G - Bombus terrestris, L - Lasioglossum subfasciatum. Vol. 56 No. 2 2012 Journal of Apicultural Science 101

was the lowest there, across all habitats altogether accounted for 68.2% of the studied. The most numerous family was assemblage. The H’ index reached a value Apidae (10 species, 93 individuals) (Tab. 1, of 3.66, while the index of evenness was 2). The H’ and J’ indices were 3.59 and 0.82 (Tab. 3). 0.57, respectively (Tab. 3). Tree canopies - There were 17 individuals Ground cover - The bees captured representing 8 species (Tab. 3). Eudominant in this layer belonged to 22 species species were Apis mellifera (53%) and (Tab. 3). Among the 104 individuals, Bombus lucorum (11.8%), and dominant there was a predominance of Apidae: species were Andrena nitida (5.9%), Apis mellifera (28.8%), Bombus lucorum Osmia rufa (5.9%), B. hortorum (5.9%), (9.6%), B. pratorum (7.7%), B. rupestris B. hypnorum (5.9%), B. pascuorum (5.9%) (7.7%), and B. pascuorum (6.7%) as well and B. pratorum (5.9%) (Fig. 6). The index as Macropis europaea (7.7%) from the of species diversity was 2.29, and the index family Melittidae (Fig. 6). These species of evenness was 0.76 (Tab. 3).

Ground cover Tree canopies D [%] D [%]

30 50

45 25 40

20 35 30

15 25

20 10 15

5 10 5

0 0 A C M B E I Remaining I A H C B 18 sp. Species 24,5% Species Fig. 5. Dominance patterns in bee assemblages collected in the fi r forest (BJ) in the Suchedniów- Oblęgorek Landscape Park; A - Apis mellifera, B - Bombus pascuorum, C - Bombus lucorum, E - Bombus bohemicus, H - Andrena cineraria, I - Bombus pratorum, M - Bombus sylvarum

Ground cover Tree canopies D [%] D [%]

35 60

30 50

25 40

20 30 15

20 10

5 10

0 0 A C N I O B Remaining A C R P S T B I 16 sp. Species 31,8% Species Fig. 6. Dominance patterns in bee assemblages collected in the riparian forest (LG) in the Suchedniów-Oblęgorek Landscape Park; A - Apis mellifera, B - Bombus pascuorum, C - Bombus lucorum, I - Bombus pratorum, N - Macropis europaea, O - Bombus rupestris, P - Osmia rufa, R - Andrena nitida, S - Bombus hortorum, T - Bombus hypnorum 102

Fig. 7. Similarity between bee assemblages of forest habitats in S-OLP: A – qualitative similarity, Marczewski-Steinhaus index (MS), B – quantitative similarity, Renkonen index (Re) The finding of bees in Moericke traps similarity, below 30%, was calculated for placed in two vertical layers in the study the remaining pairings of habitats (Fig. 7A). habitats indicates that bees penetrated The diagram presenting quantitative the entire vertical range of the forests. similarity of assemblage structure (based At the same time, particular layers were on the Re index) reveals decreasing penetrated more. values of this parameter, from the bee All traps placed on the forest floor assemblages found at various sites. These in ground cover, collectively caught sites were: the mixed and mesic coniferous 1192 individuals (88.8%) in all study forest sites (70%), mixed coniferous and habitats, representing 76 bee species. oak-hornbeam sites (69%) and mesic The percentages of total abundance at coniferous and oak-hornbeam sites (62%). particular sites ranged from 85.9% to Then there were the assemblages identified 90.3%. Species of the genus Bombus and in floristically poorer habitats (fir forest Andrena haemorrhoa were dominant in the and riparian forest), where the index of low-growing herb layer. Canopy layer traps quantitative similarity ranged from 51% to across the Park yielded 150 individuals 57% (Fig. 7B). belonging to 23 species and representing only 11.2% of all bee individuals captured DISCUSSION during the study. The prevailing species The finding of 76 bee species in the forests in this layer also belonged to the genera of the Suchedniów-Oblęgorek Landscape Bombus and Andrena (Tab. 1). Park (S-OLP) indicates that these habitats An analysis of species similarity of are attractive to bees. The bee assemblages assemblage structures (based on the MS in S-OLP were mainly dominated by index) found two groups. One group representatives of two genera: Bombus and was comprised of the bee assemblages Andrena. Together with their nest parasites, from the mixed coniferous forest, mesic they accounted for 48.7% of species in the coniferous forest, and oak-hornbeam assemblage. Their individuals constituted forest, with similarity exceeding 50% 59.2% of the assemblage. (51-57%). The other group was made up of As regards species preferring forest the bee assemblages of the oak-hornbeam habitats, those most commonly captured forest, fir forest, and riparian forest, with were Bombus lucorum, B. pascuorum, similarity indices of 34-39%. The lowest and B. pratorum. These species were also Vol. 56 No. 2 2012 Journal of Apicultural Science 103 classified as dominant or subdominant in 20% of all individuals in the canopy layer previous studies of forest communities of a Leucobryo-Pinetum mesic coniferous in Poland, such as oak-hornbeam forests forest in Bory Tucholskie. Krzysztofiak (Tilio-Carpinetum) or mixed and mesic (2001) found as little as 5% of all coniferous forests (Leucobryo-Pinetum, individuals in a spruce-pine stand in Wigry Peucedano-Pinetum, Calamagrostio- National Park. Pinetum) (Banaszak, 1990; The results of the present study indicate Pawlikowski, 1992; Banaszak and that each study habitat was characterised Cierzniak, 1994; Krzysztofiak, 2001). by different values of species richness, Thus, they are characteristic species closely abundance, and species diversity and associated with forest habitats. From the evenness indices. An analysis based on the other species, Andrena haemorrhoa was values of the S, H’ and J’ indices revealed also abundantly captured in the present the presence of two groups of assemblages: study. Cierzniak (2003) obtained similar a structurally-rich group where these results in a study of bee assemblages of indices reached high values and a group oak-hornbeam forests of the central part of characterised by a poorer structure and Wielkopolska. lower values of S, H’, J’. The former group, The study revealed that most bee with a diversified species composition individuals, chiefly of the genera Bombus (47-55 species), high abundance and Andrena, were captured in traps placed (227-457 individuals), and high values of in the ground cover. Krzysztofiak the H’ (4.27-4.75) and J’ (0.68-0.76) indices, (2001), who analysed the penetration of comprised the bee assemblages from the bees into different vegetation layers in mesic and mixed coniferous forest sites spruce-pine stands in Wigry National Park, and the oak-hornbeam site (Tab. 3). The also found the most intense penetration of latter group, consisting of the assemblages these bee genera into the low herbaceous from the fir forest and riparian forest plant layer in mature stands. A study by sites, was characterised by poorer species Banaszak and Cierzniak (1994) found richness (22-24 species), low abundance twice as many bee species in the herb layer (121-129 individuals), and low values of the than in tree canopies in oak-hornbeam H’ (3.48-3.59) and J’ (0.56-0.57) indices. and pine stands. Similar results were also The same patterns were observed for bee obtained by Kriger and Cierzniak assemblages captured in the different (2006) in a mesic coniferous forest of Bory layers, i.e. ground cover and tree canopies, Tucholskie National Park. in each study habitat (Tab. 3). In the present study of forest communities Abundance and species richness as in S-OLP, tree canopies did not support well as species diversity and evenness abundant bee assemblages. Most were found to be lower in the riparian and individuals preferred to use the sub-canopy fir forest habitats than in the mesic and layer, where vegetation density was low, mixed coniferous forest and oak-hornbeam from 10% in the mesic coniferous forest to forest sites. Qualitative and quantitative 40% in the mixed coniferous forest, oak- similarity was also seen to decrease from hornbeam forest and riparian forest, the the bee assemblages in the mesic and bees were able to move fast in that zone. mixed coniferous and oak-hornbeam forest Kriger and Cierzniak (2006) state that habitats to those in the fir and riparian bees captured in tree canopies use gaps forest sites. For bees, the low attractiveness and large spaces between trees to move of the riparian and fir forest habitats was into adjacent areas in search of food. Food- related to the spatial structure of the stand driven migrations are common among bees and species composition of ground cover, in forest habitats in view of the insufficient with decreasing abundance of flowering supply of food in this biotope. Kriger and plants and attractive nesting sites. Cierzniak (2006) caught approximately 104

Pawlikowski (1985) states that the Banaszak J., Plewka T. (1981) - Apoidea food base is a determinant of habitat (Hymenoptera) Kampinoskiego Parku attractiveness for bees. Other equally Narodowego. Fragm. faun., 25, 24: 435-452. important factors include physical factors, Bąk J. (2003) - Trzmiele (Bombus Latr.) i such as the microclimate, and a type of trzmielce (Psithyrus Lep.) (Hymenoptera, substrate that promotes nesting. It appears Apidae) w wybranych fitocenozach that both a dwindling food base and habitat Suchedniowsko-Oblęgorskiego Parku conditions (e.g. substrate moisture levels), Krajobrazowego. Prądnik 13: 235-244. which changed in the sequence of plant Cierzniak T. (2003) - Ekologia pszczół w communities presented above, might have dynamicznym kręgu zbiorowisk grądowych. influenced the abundance and species Wyd. Akad. Bydgoskiej, Bydgoszcz. richness of bee assemblages. Similar conclusions were drawn by Kosior and Dylewska M. (1966) - The Apoidea of the Fijał (1992) in their study of bees of Babia Góra Mountain. Acta zool. cracov., the Zamość region. They analysed the 11 (5): 111-179. structure of bee assemblages in open, semi- Dylewska M., Noskiewicz J. (1963) - open (ecotone), and forest habitats to find Apoidea of the Pieniny National Park. Part II. that the degree of organisation of these Colletidae, Andrenidae, Halictidae, Melittidae, assemblages (reflected in high values of Apidae (Nomada SCOP.). Acta zool. cracov., S, H’, and J’ indices) was lowest in forest 13: 477-532. habitats and increased in open and more Enghoff H., Nielsen E. S. (1978) - An sun-exposed areas. U.T.M. base map of the Western Palearctic In view of the attractiveness of the Region for mapping of faunistic data. Entomol. Suchedniów-Oblęgorek Landscape Park Meddr., 46: 71-72. and the diversity of habitats in this area, Kondracki J. (2002) - Geografia regionalna studies of bee assemblages are being Polski, PWN, Warszawa. continued there. Kosior A., Fijał J. (1992) - Analiza REFERENCES faunistyczno-ekologiczna owadów pszczoło- watych Apoidea województwa zamojskiego. Banaszak J. (1987) - Pszczoły (Hymenoptera, Stud. Ośr. Dok. Fizjogr., 20: 13-52. Apoidea) wybranych zespołów roślinnych Kriger R., Cierzniak T. (2006) - Zmiany Wielkopolskiego Parku Narodowego. Bad. sukcesyjne zgrupowań pszczół (Apoidea) fizjogr. Pol. Zach., 35: 5-23. w borach Leucobryo-Pinetum w Parku Banaszak J. (1990) - Pszczoły (Apoidea) Narodowym Bory Tucholskie, in: J. grądów i dąbrów świetlistych Niziny Banaszak, K. Tobolski (ed.). Park Narodowy Mazowieckiej. Zesz. nauk. WSP, Bydgoszcz, Bory Tucholskie u progu nowej dekady. Wyd. 8: 23-35. Uczeln. UKW w Bydgoszczy, Bydgoszcz, pp. Banaszak J. (2004) - Pszczoły (Apidae), in: 319-345. W. Bogdanowicz, E.Chudzicka, I. Pilipiuk, E. Krzysztofiak A. (2001) - Struktura Skibińska (ed.). Fauna Polski. Charakterystyka zgrupowań pszczół (Apoidea, Hymenoptera) w i wykaz gatunków, Muzeum i Instytut Zoologii różnowiekowych drzewostanach świerkowo- PAN, Warszawa, pp. 346-362. sosnowych Wigierskiego Parku Narodowego. Banaszak J., Cierzniak T. (1994) - Spatial Zesz. nauk. Akad. Bydgoskiej, Stud. Przyr., 15: and temporal differentiation of bees (Apoidea) 113-215. in the forests of Wielkopolski National Park, Marczewski E., Steinhaus H. (1959) - O Western Poland. Acta Univ. Lodz., Folia Zool., odległości systematycznej biotopów. Zast. 2: 3-28. Mat., 4: 195-203. Banaszak J., Jaroszewicz B. (2009) - Bees Michener C. D. (2007) - The Bees of the of the Białowieża National Park and adjacent World, John Hopkins University Press, area. NE Poland (Hymenoptera: Apoidea, Baltimore-London. Apiformes). Pol. pismo entomol., 78: 281-313. Vol. 56 No. 2 2012 Journal of Apicultural Science 105

Mirek Z., Piękoś-Mirkowa H., Zając A., Pielou E. C. (1966) - Species diversity and Zając M. (2002) - Flowering plants pattern - diversity in the study of ecological and pteridophytes of Poland - a checklist. succesion. J. Theor. Biol., 10: 370-383. Krytyczna lista roślin naczyniowych Polski, Renkonen O. (1938) - Statistisch-ökologische Szafer W. Institute of Botany, Pol. Acad. Sci., Untersuchungen über die terrestische Käferwelt Kraków. der finnischen Bruchmoore. An. Zool. Soc., 6: Moericke V. (1951) - Eine Farbfalle zur 1-231. Kontrolle des Fluges von Blättläusen, Romer E. (1949) - Regiony klimatyczne insbesondere der Pfirsichblattlaus, Myzodes Polski. Pr. Wroc. Tow. Nauk., Ser. B. 16. persicae (Sulz.). Nachrbl. Dtsch. Pflzchutzd., Ruszkowski A., Ruszkowski J. (1998) 3: 23-24. - Słownik polskich nazw owadów. Cz. I, Oertli S., Müller A., Dorn S. (2005) Instytut Sadownictwa i Kwiaciarstwa - Oddział - Ecological and seasonal patterns in the Pszczelnictwa, Puławy. diversity of a species-rich bee assemblage Shannon C. E., Weaver W. (1963) - (Hymenoptera: Apoidea: Apiformes). Eur. J. The mathematical theory of communication, Entomol., 102: 53-63. University Illinois Mi, Urbana. Pawlikowski T. (1985) - Zgrupowania dzikich Tuell J. K., Isaacs R. (2009) - Elevated pszczołowatych (Hymenoptera, Apoidea) na pan traps to monitor bees in flowering crop kserotermicznych siedliskach wydmowych canopies, Entomol. Exp. Appl., 131: 93-98. Kotliny Toruńskiej. Stud. Soc. Scient. Tor., 10, 4: 1-57. Witkowski Z. (1975) - Ekologia i sukcesja ryjkowców (Coleoptera, Curculionidae) łąk Pawlikowski T. (1990) - Funkcja zespołów kośnych okolic Zabierzowa, PWN, Warszawa. pszczołowatych w różnowiekowych monokulturach sosnowych Kotliny Toruńskiej. Wyd. SGGW-AR, 42: 184-191. Pawlikowski T. (1992) - Struktura zespołów pszczołowatych (Hymenoptera, Apoidea) na obszarach leśnych Kotliny Toruńskiej. Rozprawy UMK, Toruń. PRZESTRZENNE ZRÓŻNICOWANIE ZGRUPOWAŃ PSZCZÓŁ (HYMENOPTERA: APOIDEA: APIFORMES) W ZBIOROWISKACH LEŚNYCH SUCHEDNIOWSKO-OBLĘGORSKIEGO PARKU KRAJOBRAZOWEGO

Bąk-Badowska J.

Streszczenie Celem badań prowadzonych w latach 2004-2005, od kwietnia do października było scharakteryzowanie zgrupowań pszczół (Apiformes) w zróżnicowanych fi tosocjologicznie zbiorowiskach leśnych Suchedniowsko-Oblęgorskiego Parku Krajobrazowego. Do odłowu zastosowano metodę pułapek barwnych Moerick’ego. Strukturę każdego zgrupowania określano: liczbą prób (n), liczbą gatunków (S), liczbą osobników (N), dominacją (D), ogólnym zróżnicowaniem gatunkowym (H’) oraz równocennością gatunkową (J’). Do jakościowego porównania wyróżnionych zgrupowań posłużono się wskaźnikiem Marczewskiego-Steinhausa (MS), a podobieństwo ilościowe badano za pomocą wskaźnika Renkonena (Re). 106

Na pięciu powierzchniach badawczych odnotowano 76 gatunków pszczół, wśród których dominowali przedstawiciele rodzin Apidae (28 gat., 900 os.) i Andrenidae (20 gat., 222 os.). Należały do nich: Apis mellifera (24,5%), Bombus lucorum (9,1%), B. pascuorum (8,8%) i Andrena haemorrhoa (5,4%). Wskaźniki różnorodności gatunkowej H’ i równocenności J’ osiągnęły najwyższe wartości w borze mieszanym (BM), odpowiednio 4,75 i 0,76 a najniższe w borze jodłowym (BJ), wynoszące 3,48 i 0,56. Podobieństwo jakościowe i ilościowe struktury zgrupowań spadało począwszy od środowisk boru mieszanego, świeżego i grądu do środowisk o uboższym składzie fl orystycznym i niesprzyjających warunkach do gniazdowania, czyli boru jodłowego i łęgu. W pułapkach umieszczonych na dnie lasu w runie, stwierdzono więcej osobników i gatunków pszczół - 1192 os. (88,8%) i 76 gat., niż w warstwie koron drzew - 150 os. (11,2%) i 23 gat. Dotyczyło to wszystkich środowisk leśnych S-OPK. Słowa kluczowe: Apiformes, struktura zgrupowań, środowiska leśne, Suchedniowsko- Oblęgorski Park Krajobrazowy, rozmieszczenie pionowe.