Reproduction and Accompanying Fauna of Red Mason Bee Osmia rufa L. (syn. Osmia bicornis L.) in Areas with Different Levels of Urbanization

Urban expansion causes the destruction and fragmentation of natural habitats (Kearns et al., 1998; Biesmeijer et al., 2006; Ewers & Didham, 2006), which has a negative impact on their biodiversity (McKinney, 2002). More than 80% of urban areas are large impermeable surfaces such as buildings, roads and sidewalks, which limit the access of plants and animals to soil and water and prevent their migration (Blair & Launer, 1997).

Urbanization also increases the loss of native species (Czech et al., 2000) and the spread of alien species, as the site of Adelaide, a city in southern Australia, where 132 of the total number of native species have died out locally and 648 alien species (mostly plants) have arrived. The process of replacing native species with foreign species leads to the homogenization of ecosystems, which has been observed in the case of birds and butterflies (Blair, 2001). The number of non-native species is increasing while the native species are decreasing in urban centers, which is related to the “urban-rural gradient” (Blair & Launer, 1997). Changes in the urban landscape reduce the number of bird species (Savard et al., 2000) and mammals (Tait et al., 2005), especially in isolated areas. Fragmentation causes changes in the structure of species dominance, which indicates a tendency to form mono-dominants, e.g. bumblebees and butterflies (Eremeeva & Sushchev, 2005).

Many studies have confirmed that pollinator diversity and abundance were significantly negatively associated with higher urbanization levels (McIntyre & Hostetler, 2001; Zanette et al., 2005; Bates et al., 2012). Cardoso & Gonçalves (2018) showed that the richness of bee species decreased by 45% over thirty-four years. Fitch et al. (2019) documented a change in the gender ratio of ground-nesting bees along an urbanization gradient (reduction in the number of females in the city compared to urban and rural areas). Urban areas are characterized by a large spatial diversity of habitats (Savard et al., 2000; Thompson et al., 2003), which may have a positive effect on the development of space-requiring organisms, including some plant and invertebrate species (McKinney, 2008).

Green areas, and in particular the housing-estate garden, retain a surprising richness and abundance of bee species (Normandin et al., 2017). Many studies confirm that cities are inhabited by many species (Banaszak-Cibicka & Żmihorski, 2012; Baldock et al., 2015; Cariveau & Winfree, 2015; Sirohi et al., 2015; Threlfall et al., 2015; Hall et al., 2017). The occurrence of bees depends on various factors, most importantly the availability of food but also the presence of suitable breeding places. Research has shown that plant-species diversity is greater in cities than in surrounding rural areas (McKinney, 2002; Wania et al., 2006). Many different species of ornamental and exotic plants can be found in parks and gardens (Thompson et al., 2003; Frankie et al., 2005) which provide bees with sufficient nourishment. The attractiveness of the local flora causes feeding-ground activity and the number of pollen and nectar collectors to be higher suburban gardens, than in forests and plantations (Kaluza et al., 2016). The red mason bee (Osmia rufa L.), one of the most common early spring species in Poland with broad food preferences (Ruszkowski & Biliński, 1986; Teper, 2007), readily occupies artificial nests and forms aggregations (Giejdasz & Wilkaniec, 2003) to pollinate many agricultural and horticultural crops (Biliński & Teper, 2004, 2009; Fliszkiewicz et al., 2011). Osmia rufa was recently introduced as an environmental complement (Everaars et al., 2011; MacIvor & Packer, 2016) and is used as a bioindicator (Szentgyörgyi et al., 2017). An important factor influencing the health and number of red masons is the accompanying fauna, including nest parasites. Many such species as Cacoxenus indagator (Loew, 1858) (Drosophilidae), Monodontomerus obscurus (Westwood, 1833) (Torymidae) and Chaetodactylus osmiae (Dufour, 1839) (Chaetodactylidae) parasitize on red mason broods or pollen provision and reduce the bee population by 50% or, in extreme cases even by 95% (Krunić et al., 2001, 2005). Osmia rufa nests can have many random residents, nest destroyers, cleptobionts or predators (Krunić et al, 2005), including rare and useful insect species (Zajdel et al., 2015). The abundance and biodiversity of Osmia rufa accompanying fauna depends on the abundance of bees (Krunić et al, 2005), the selection of cocoons, nest usage (Madras-Majewska et al., 2011) and the nesting time of bees at the site (Zajdel et al., 2014). Recently, Łoś et al. (2020) studied masonry beess reproductive success along an urbanization gradient, as well as their pathogens and nest parasites. This work was a benchmark for the results of our study.

Our research presents a data set on the studied population of Osmia rufa in areas with different urbanization levels: a city, suburbs and villages. The paper concentrates on the study of solitary bee reproduction parameters but also analyzes the biodiversity of fauna accompanying the nest. We verified two global hypotheses; the first concerned the identification of potential differences between habitats while the second differences between urbanization levels. We checked in which habitats and areas (1) more cocoons and higher population growth had been obtained, (2) more larvae and pupae had died, (3) more losses had been caused by nesting parasites and (4) higher biodiversity of accompanying fauna had been.

Variation in species richness, especially in the Apoidea superfamily, occurs in all biotopes of the urbanization gradient from rural areas to urban agglomerations (Ahrné et al., 2009; Fetrige et al., 2008; Matteson et al., 2008; Banaszak-Cibicka & Żmihorski, 2012; Fortel et al., 2014; Hudewenz & Klein, 2015; Verboven et al., 2014; Baldock et al., 2015; Cariveau & Winfree, 2015; Sirohi et al., 2015; Threlfall et al., 2015; Hall et al., 2017). Urbanization may negatively affect individuals and bee diversity (Bates et al., 2011). Asymmetry of body can be caused by environmental pollution, parasites and food shortages (De Anna et al., 2013). Banaszak-Cibicka et al. (2018) concluded that the body size of bees did not differ among urban, suburban and rural habitats, and urban bees were less asymmetric compared to bees found in rural areas. This proves that, the urban landscape provides bees with quality habitats.

We investigated only one species of bees, Osmia rufa, but their afterborn nest material was meticulous examined for three years. A different number of cocoons were obtained from the urban, suburbs and rural within the habitats. Łoś et al. (2020) found that urban sites have the highest indices of reproductive success and the lowest number of breeding failures compared to suburban and rural sites. Our research has shown that Osmia rufa population develop just as well in every area regardless of the level of urbanization. Good reproductive results of red mason bee are evidenced by the high emergence rate, i.e. the percentage of bees that emerged cocoons in spring. In all areas types, the index was always above 90%. Other studies show that the habitat type has a significant influence on reproductive performance (Fliszkiewicz et al., 2014). In our research, nests were located in landscapes strongly transformed by man, both in the city (streets, high buildings) and in the countryside (large agricultural areas), and yet population growth in all habitats was almost five times higher than the number of initially placed cocoons. These results seem to be very high, compared to the results by Fliszkiewicz et al. (2014) who had achieved a much lower reproduction grow rate than ours although in such more favorable landscapes as a meadow or an orchard, 3.91 and 3.17 respectively.

We showed that the mortality of red mason larvae and pupae was habitat dependent. Although the highest mean mortality was in the city, the mean in the suburbs and the lowest in the countryside, we found no significant differences between areas with different urbanization levels. However, Łoś et al. (2020) found that the sites in the city had a lower number of “mummies” (dead larvae) than suburban and rural habitats.

Although our research showed that the level of urbanization did significantly affect the number of cocoons and brood mortality, we obtained the results at the statistical trend level. In our research, we had a small number of repetitions. We can assume that if we had performed the study on a larger number of habitats, we would have obtained statistical differences among areas with different levels of urbanization.

Red mason bee nests are inhabited by various species of insects and arachnids. Some of them belong to the ever-present accompanying fauna - C. indagator, M. obscurus and Ch. osmiae (Krunić et al., 1995; Krunić et al., 2005; Fliszkiewicz et al., 2012; Zajdel et al., 2014; Zajdel et al., 2015) and most often contribute to the death of the brood. Although the parasite damage in the suburbs was almost three times higher than in the city and the countryside, we found no significant differences between the suburbs and villages. The presence of parasites is negatively correlated with reproductive success and may be a limiting factor for the O. rufa population (Łoś et al., 2020). In the future, it would be useful to investigate why parasites occupy so many breeding chambers in peri-urban areas, with particular emphasis on habitat fragmentation and the presence of flowering plants in the habitat along an urbanization gradient. According to Goodell (2003), limited access to the food base may affect the reproductive success and intensify parasitism. Furthermore, pollen availability is very important for body size (Johnson, 1988; Bosch & Vicens, 2002; Seidelmann, 2006) and increases the efficiency of pollination work and affects reproductive performance (Seidelmann et al., 2010).

There are not many studies that show that the habitat type (Fliszkiewicz et al., 2012; 2014) and urbanization level (Łoś et al., 2020) have a significant influence on the reproductive performance of Osmia rufa. In our research, nests were located in a landscape strongly transformed by man, both in the city with streets and high buildings and in the countryside with large agricultural areas, and yet population growth in all habitats was high, in comparison with different more natural habitats including forest, meadows and gardens (Fliszkiewicz et al., 2014). The red mason bees has a small flight range (Radmacher & Strohm, 2010) and this may be the reason for its success in fragmented habitats, as long as they find food (Goodell, 2003; Seidelmann, 2006).

Our research shows that despite the changes brought about by urbanization and agriculture, Osmia rufa show great flexibility and adaptability to new conditions. Additional studies in other bee species and habitats are required to discover if these findings are more widely applicable.