Early Floral Resources for Urban Bees From Ornamental Shrubs Ribes Aureum, Ribes Sanguineum and Staphylea Pinnata

Bees are principal contributors to pollination services in both the natural and anthropogenic habitats (Klein et al., 2007). Insect pollination is a key factor in seed and fruit yield, ensuring the reproduction of plant species and providing food for humans and wildlife. In the past decade, one of the fastest emerging traditions in cities has been urban agriculture, including beekeeping (Peters, 2012; Marìn et al., 2019). Urban agriculture provides such multiple benefits as food production, relaxation and the saving of cultural heritage (Marìn et al., 2019). However, such activities require proper “bee-friendly” management of urban areas, including the selection and use of plants for example valuable nectar and pollen resources. Urban areas contain patches of unused land including road verges or ruderal areas and such amenity areas as parks, lawns and roofs. This is a potential to alter the management of this land and to create an attractive flower-rich landscape thus increasing food pasture for insect pollinators, including bees (Matteson, Grace & Minor, 2013; Larcher et al. 2017). Ornamental plants can provide insects with considerable amounts of nectar and pollen and contribute to the diversity of food resources within cities (Garbuzov & Ratnieks, 2014; Masierowska et al., 2018; Jachuła et al., 2019).

The warming Urban Heat Island effect, increased water stress and pollution contribute to cities’ specific environmental conditions (Pickett et al., 2011) and may affect plant-pollinators relations. Spring-flowering plants tend to advance their blooming in urban habitats (Neil & Wu, 2006). Honeybees, queen bumblebees and solitary bees are active early in the year in cities (Hicks et al., 2016). Spring is a period of high nutritional demand for spring-emerging bees, which lose a lot of weight during over-wintering in response to warm winters (Fründ, Zieger, & Tscharntke, 2013). Thus, an adequate quality and quantity of early floral resources is vital for their development and activity. Spring forage limitation is currently considered as a possible driver of the negative impact of urbanization on bees (Harrison & Winfree, 2015). Early in the year (April-May), nectar and pollen are usually provided by native perennial weeds (Denisow, 2011), which are problematic from the aesthetic point of view. Thus, incorporating ornamental trees, shrubs or flowers into green space landscaping can enhance both the availability of early season resources to urban bees and the aesthetic value of the urban landscape.

The attractiveness of plants to insects depends on the traits of flower morphology and colour, pollen and nectar quality (Garbuzov & Ratnieks, 2014), flowering pattern and floral-display size (Thompson, 2001) and these should be considered when selecting plants for bee pasture. The aim of this study was to evaluate three shrubs Ribes aureum Pursh., Ribes sanquineum Pursh., and Staphylea pinnata L. as early food resources for urban bees and more specifically to determine (i) the abundance and flowering pattern, (ii) the nectar and pollen production, and (iii) the spectrum of urban insect visitors, in particular bees. The Ribes species are the drought-tolerant shrubs with high aesthetic value (Borowski et al., 2016; Muras, 2017). Staphylea pinnata is a native species with original flowers and fruits, and in the past plants of the species were transferred from natural stands and planted in gardens. Moreover, this species is light and soil tolerant (Dolatowski & Seneta, 2020).

Since studies on the apiarian value of ornamental Ribes species in SE Poland in the 1990s (Masierowska, 1993; 1995), the attractiveness of these shrubs to urban pollinators has not been studied despite common changes in the urban environment, including the UHI effect, altered precipitation or land-use change, noted also in the city studied here (Rysiak & Czarnecka, 2018). The attractiveness of S. pinnata has never been evaluated, although it is listed as a melliferous plant in Poland (Lipiński, 2010).

Early spring is when both managed and wild bees have a high nutritional demand (Dick et al., 2015; Moquet et al., 2015), but also when there is often a shortage of nectar and pollen food (Lipiński, 2010; Denisow, 2011). However, thanks to the proper selection of plants, such urban flora as ornamental shrubs and trees (Somme et al., 2016) can provide bee species with a variety and continuity of floral resources and create good conditions for urban agriculture, including beekeeping. The results of this study expand the list of early-spring flowering shrubs that are useful for urban pollinators, including honeybees and bumblebees.

In all the plants observed in this study, the onset and length of blooming depended on weather conditions prevailing during the growing seasons and were probably affected by urban warming – a phenomenon recently confirmed for Lublin by Rysiak & Czarnecka (2018). At high temperatures, the investigated shrubs, in particular R. sanguineum, advanced their blooming and had a shorter blooming period. In 1990s, when no urban warming was reported in the Lublin area, R. sanguineum and R. aureum flowered nearly two weeks later (mid-April-mid-May) (Masierowska, 1995) than in the present study. In Poland in natural stands, S. pinnata blooms in May and June (Rutkowski, 2006) while recently in Lublin in late April–May. Spring-blooming and insect-pollinated plants tend to be more sensitive to urbanization and usually advance their blooming, although many plant species do not show significant changes in flowering (see Neil & Wu, 2006). A change in flowering time may lead to an asynchronous phenological mismatch between plants and their insect pollinators (Solga et al., 2014). Pollinators emerging after plant bloom might experience a decreased food supply, and plants that bloom before their pollinators are active may face pollination limitation (Fagan et al., 2014). A few experimental studies have found that both spring bees and the plants visited by them seem to advance their seasonal phenologies at similar rates and so avoid such a mismatch (Bartomeus et al., 2011; 2013). However, the phenological changes and their consequences are extremely species–specific (Solga et al., 2014) and need further investigations.

The studied species produced thousands of flowers gathered in inflorescences. In mass-flowering plants, the inflorescence rather than a single flower is a fundamental unit of pollinators’ attraction, and the display of multiple flowers in the inflorescence increases plants’ attractiveness to flower visitors (Harder et al., 2004). Despite the considerable differences in the number of flowers, the inflorescences of the studied species exhibit quite a similar pattern of flower presentation. They are characterized by continuous flower opening with a peak during the first days of blooming. By displaying numerous flowers from the beginning of bloom, the plant attracts inexperienced bees and encourages experienced ones to revisit (Makino & Sakai, 2007). Thus, it obtains the services of faithful visitors that will continue to visit despite subsequent decreases in the rate of flower production (Thomson, 1985). Moreover, displaying many flowers might increase the likelihood of the plant being discovered by pollinators quickly (Makino & Sakai, 2007).

The flowers in the studied species persisted for five to nine days on average. Their inflorescences lived up to 2.7 weeks. A prolonged flower and inflorescence lifespan appears to be of a great value to floral visitors, as it increases the size and length of floral display and thus extends the food supply (Willmer, 2011).

The studied species bloomed abundantly, in particular S. pinnata - the biggest shrub among the plants under study. The lowest number of flowers was produced by R. sanguineum, but their blooming abundance was relatively consistent throughout the years of the study. This matters when the aesthetic attractiveness of plants is considered before planting. In the other shrubs, there were more pronounced seasonal differences in the total number of flowers · plant⁻¹. Seasonal differences in flowering abundance have been reported for many ornamental species grown in urban habitats and mainly attributed to meteorological factors but also to species tendency to alternation of blooming (Denisow, 2002; Masierowska et al., 2018). This phenomenon is likely to be responsible for the major differences in the flowering abundance of R. aureum and S. pinnata in the consecutive years of the study, but a longer period of observation is necessary to prove this assumption. Hymenopterans were the principal visitors to the flowers of the studied species. R. sanguineum attracted bumblebees, which is consistent with observations reported by Ostrowska (1981), and S. pinnata attracted mainly honeybees, as demonstrated by Lipiński (2010). However, Knuth (1908) reported that flies from the Syrphidae and Muscidae families were the only visitors to flowers of this species. In the present study, syrphid flies were never the dominant visitors to S. pinnata, although they accounted for 21% of all the insect visits in 2014. The proportions of bumblebees and honeybees visiting R. aureum flowers were similar but slightly fluctuated in the years of the study. In Poland, Ruszkowski (1998) listed R. aureum among indicator food plants for Bombus hortorum, B. ruderalis, and B. subterraneus, confirming its attractiveness to bumblebees. Knuth (1908) and Lipiński (2010) reported a minor interest of honeybees in R. aureum flowers and both authors attributed it to deeply concealed nectar. As shown by Lipiński (2010), honeybees are able to collect the nectar of this plant only through holes bitten in the tubular hypanthia by short-tongued bumblebees (secondary nectar robbing). In the present study, the R. aureum flowers produced a considerable amount of nectar filling the hypanthium tubes, which could be reached in a legitimate way by such bees with short mouthparts as A. mellifera. A similar mechanism was observed in honeybees visiting long-corolla Lonicera species (Jachuła et al., 2019). In the recent study, no nectar robbing on Ribes flowers was observed. However, bees more eagerly visited older R. aureum flowers than newly opened ones, probably due to the higher amounts of accumulated nectar.

Besides their high aesthetic value, both Ribes species and S. pinnata should be considered as additional nectar and pollen resources for bees. In the climatic conditions of SE Poland, the studied shrubs provide food from late March to late May. This may be important for bees with early activity in the urban environment, including honeybees, queen bumblebees, and solitary bees such as Andrena, Halictus, or Osmia (Hicks et al., 2016). The nectar-sugar quantities secreted in nectar per a single flower of R. aureum, R. sanguineum and S. pinnata were 1.5, 0.8 and 1.6 mg, respectively. Overall, most nectar characteristics for R. aureum and R. sanguineum were lower than the values previously reported in SE Poland (Masierowska, 1993; 1995). However, this is more than the nectar sugar amount · flower⁻¹ found for Salix (0.02–0.06 mg) (Koter, 1987) or Acer (~ 0.46 mg) and Aesculus (0.16–0.28 mg) species (Somme et al., 2016), early spring/spring flowering shrubs and trees recommended for urban greenery planning. The surveyed shrubs provide moderately concentrated nectar although the values ranged from 15–50%, which corroborates the results of previous studies on R. aureum and R. sanguineum (26–31% on average) (Masierowska, 1993, 1995). Such nectar offers highly needed energy for such nectar consumers as flies and short- and long- tongued bees (Willmer, 2011). Indeed, both hymenopterans and dipterans were visitors to the Ribes and S. pinnata flowers in this study.

The amount of pollen available for insects from a single flower in all the species was small (0.4–0.8 mg) but similar to the values reported for the flowers of Aesculus (Warakomska, 1972) and Crataegus species (Szklanowska, 1992), which are commonly planted in cities. For both Ribes species, the pollen amount · flower⁻¹ was similar to the values reported in previous studies (Masierowska, 1993; 1995). For the first time, honeybees and bumblebees have been found to collect willingly S. pinnata pollen. Bees’ pollen loads from R. aureum and R. sanguineum were described by Ostrowska (1981) and Hodges (1984).

The studied species produced a considerable number of flowers which resulted in a relatively high estimated sugar yield · plant⁻¹ in the range of 4.3–92.9 g and pollen yield · plant⁻¹ of 1.8–44.0 g (on average in both cases, R. sanguineum – S. pinnata, respectively). Due to the most abundant flowering and the high sugar nectar and pollen productivity of flowers, the estimated sugar and pollen yield · plant⁻¹ in S. pinnata was much higher than the values calculated for the other taxa. Moreover, the sugar yield provided by this shrub was higher than that found for Lonicera tatarica and L. maackii (46.9–63.4 g · plant⁻¹, respectively), which flower simultaneously with S. pinnata and are a good source of nectar sugars for urban bees in SE Poland (Jachuła et al., 2019). The estimated sugar yield and pollen yield in both Ribes species (4.3–19.8 g· and 1.8–6.1 g·, respectively) was in a range of values found previously in the Lublin area (4.3–34.7 g and 0.5–8.6 g, respectively) (Masierowska, unpub. data).

In conclusion, R. aureum, R. sanguineum, and pinnata shrubs can be considered as additional early floral food resources for urban bees. The studied species exhibit many such valuable features as abundant and extended flowering, skewed inflorescence flowering pattern, persistent flowers and inflorescences, and nectar and pollen reward (S. pinnata in particular). When planted among urban greenery, they may help to achieve an ornamental effect, enrich bee pasture and improve bee nutrition in the early spring/spring period. Finally, a wider use of R. aureum, R. sanguineum, and S. pinnata in the urban landscape of Poland is recommended.