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Pollination Efficiency and Foraging Behaviour of Honey Bees and Non Agricultural and Forest Entomology (2019), DOI: 10.1111/afe.12363 Pollination efficiency and foraging behaviour of honey bees and non-Apis bees to sweet cherry Maxime Eeraerts , Ruben Vanderhaegen, Guy Smagghe and Ivan Meeus Department of Plant and Crops, Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, 9000 Ghent, Belgium Abstract 1 Crop pollination generally increases with pollinator diversity and wild pollinator visitation. To optimize crop pollination, it is necessary to investigate the pollination contribution of different pollinator species. In the present study, we examined this contribution of honey bees and non-Apis bees (bumble bees, mason bees and other solitary bees) in sweet cherry. 2 We assessed the pollination efficiency (fruit set of flowers receiving only one visit) and foraging behaviour (flower visitation rate, probability of tree change, probability of row change and contact with the stigma) of honey bees and different types of non-Apis bees. 3 Single visit pollination efficiency on sweet cherry was higher for both mason bees and solitary bees compared with bumble bees and honey bees. The different measures of foraging behaviour were variable among non-Apis bees and honey bees. Adding to their high single visit efficiency, mason bees also visited significantly more flowerper minute, and they had a high probability of tree change and a high probability to contact the stigma. 4 The results of the present study highlight the higher pollination performance of solitary bees and especially mason bees compared with bumble bees and honey bees. Management to support species with high pollination efficiency and effective foraging behaviour will promote crop pollination. Keywords Apis mellifera, bumble bees, fruit set, Osmia cornuta, Prunus avium, solitary bees. Introduction implemented to support these species and their corresponding pollination service (Garibaldi et al., 2014). The western honey bee (Apis mellifera) is the principal insect Different parameters can determine the pollination perfor- species used for pollination of agricultural crops. Yield of crops mance of a pollinator species. First, at the level of a single flower, that depend on insect mediated pollination increases with pol- pollination efficiency and flower handling can indicate which linator diversity and crop visitation rates of wild pollinating pollinator species a flower visit will result in a successful polli- insects, whereas honey bee visitation rates only show a sig- nation of that flower. In several studies, the pollination efficiency nificant positive relationship in three of the 22 studied crops on a single visit basis for certain wild bee species was found to be (Garibaldi et al., 2013). Currently, consensus about clear man- higher compared with that of honey bees in certain crop systems agement strategies to optimize insect mediated crop pollination (Kendall & Smith, 1975; Kuhn & Ambrose, 1984; Bosch & Blas, is lacking (Isaacs et al., 2017; Rollin & Garibaldi, 2019). To 1994; Vicens & Bosch, 2000a; Monzon et al., 2004; Greenleaf & optimize crop pollination, it is necessary to identify which polli- Kremen, 2006; Zhang et al., 2015). In addition, compared with nator species contribute significantly to the pollination of certain honey bees, both pollen deposition on the stigma and the growth crops. Consequently, when these efficient pollinator species are of the pollen tube were found to be more favourable for cer- identified, targeted measures in and around crop fields canbe tain wild pollinators in a variety of crops (Willmer et al., 1994; Thomson & Goodell, 2001; Javorek et al., 2002; Winfree et al., Correspondence: Maxime Eeraerts. Tel.: +32 495 83 59 54; e-mail: 2007; Brittain et al., 2013; Zhang et al., 2015). However, honey [email protected] bees are also found to enhance pollen deposition in a number © 2019 The Royal Entomological Society 2 M. Eeraerts et al. of crop systems compared with certain wild pollinators (Rader pear, etc.). Pollination performance was measured as foraging et al., 2009; Wist & Davis, 2013; Sáez et al., 2014). It is clear behaviour (flower visitation rate, probability of tree change, that this pollination efficiency depends on the specific crop and probability of row change and contact between pollinator and also on the pollinating insects for which this comparison is made. the stigma) and as pollination efficiency (fruit set of flowers that Clearly, the deposition of compatible pollen and a morpholog- received only one visit). We compared these pollination perfor- ical match between the crop flower and the pollinating insect mance parameters between different types of bees: bumble bees are important aspects for understanding the pollination efficiency (Bombus spp.), honey bees, the European orchard bee (Osmia of a pollinator species (Free, 1993; Blüthgen & Klein, 2011; cornuta) and other solitary bees (mainly mining bees, Andrena Garibaldi et al., 2015). In a variety of Rosacea fruit crops, certain spp.). solitary bees (Osmia spp. and Andrena spp.) also handle flowers more effectively compared with honey bees because these soli- tary bees make more contact with the floral stigma to facilitate Materials and methods pollen deposition (Free, 1993; Bosch & Blas, 1994; Vicens & Bosch, 2000a; Monzon et al., 2004; Martins et al., 2015). The Study system foraging behaviour of pollinators is another aspect to keep in The study was conducted on a commercial multi-crop farm mind when considering pollination performance of different pol- in Baardegem, Belgium, which contains a 1-ha sweet cherry linator species. For fruit crops that depend on insects to facili- orchard. All sampling was conducted in 2018 and 2019 on tate cross-pollination, compatible pollinizer cultivars are planted the sweet cherry cultivars Kordia and Regina, which are the interspersed in the same rows or in different rows of the com- most abundant cultivars in the study orchard (11 out of 20 mercial cultivar (e.g. almond, apple, sweet cherry, strawberry, rows) and in European and North-American sweet cherry etc.). In such cropping systems, it is vital that pollinating insects production in general (Quero-Garcia et al., 2017). Given the visit flowers of different plants to exchange compatible pollen excellent quality of the cherries, Kordia and Regina are the and successfully pollinate flowers. In these crop systems, bum- two cultivars of the most commercial interest. Yet, these two ble bees and mason bees have been shown to change trees or cultivars are highly dependent on insect mediated pollination plants within and between rows more often compared with honey because they are self-incompatible, and they require pollen bees (Bosch & Blas, 1994; Willmer et al., 1994; Vicens & Bosch, from a compatible cultivar to set fruit (Lech et al., 2008). Sweet 2000a; Monzon et al., 2004; Brittain et al., 2013). Visitation rate cherry has hermaphroditic flowers with an open flower and so is another important behavioural parameter because it determines the stigma and the anthers are easily accessible to pollinators the number of flowers a certain species can pollinate per unit and, as such, pollen and nectar are easy to collect. To facilitate of time. Visitation rate has been studied in a number of crops cross-pollination, fruit growers plant compatible pollinizer systems and the parameter is variable between honey bees and cultivars in separate rows of the commercial cultivars or in non-Apis bees and also among non-Apis bees there are clear dif- between the rows of the commercial cultivars (one pollinizer ferences (Chagnon et al., 1993; Vicens & Bosch, 2000a; Thom- tree for every four or five commercial trees). Other cultivars son & Goodell, 2001; Javorek et al., 2002; Rader et al., 2009; within the study orchard are Vanda, Canada Giant, Earlise, Martins et al., 2015). Bellise, Merchant, Sylvia and Lapins (all cultivars are planted in In addition to the abundance of honey bees, the commu- full rows; see Supporting information, Fig. S1). The blooming nity of pollinating insects in agricultural crops is often very period of Kordia overlaps partially with that of Regina and the diverse (Winfree et al., 2011). With the increasing importance blooming period of Sylvia overlaps with both the blooming peri- of sustainable crop pollination, it is necessary to investigate ods of both Kordia and Regina. Vanda, Canada Giant, Earlise, the pollination performance of the entire community of pol- Bellise, Merchant and Lapins have flowering periods earlier linating insects to develop management guidelines for crop than that of Kordia and Regina. Depending on the weather pollination (Garibaldi et al., 2013). Previous studies in sweet and the cultivar, it takes approximately 8–12 weeks for the cherry have highlighted the contribution of wild pollinators to cherries to develop and ripen. No manual/chemical thinning sweet cherry production (Holzschuh et al., 2012; Eeraerts et al., like in other fruit crops (apple, pear) is applied in sweet cherry 2017; Eeraerts et al., 2019b). These studies revealed that bum- cultivation. Flowers/unfertilized fruit fall occurs 2–3 weeks after ble bees and different solitary bee species (Andrena spp. and bloom and, after these 3–4 weeks, fruit set stabilizes and the Osmia spp.) make up a significant part of the pollinator commu- reduction as a result of natural abortion of cherries is very low nity next to the ever-present honey bees. However, most stud- (Hedhly et al., 2007). ies in Rosacea fruit crops that investigate
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