Bees require suitably close foraging and nesting sites to minimize travel time and energy expenditure for brood provisioning. Knowing foraging distances in persistent (‘healthy’) populations is therefore crucial for assessing harmful levels of habitat fragmentation. For small bees, such distances are poorly known because of the difficulty of individual tagging and problems with mark-recapture approaches. Using apiarist’s number tags and colour codes, we marked 2689 males and females of four oligolectic and two polylectic species of Osmiini bees (Megachilidae, genera Chelostoma, Heriades, Hoplitis, Osmia) with body lengths of 6 to 15 mm. The work was carried out in 21 ha-large urban garden that harbours at least 106 species of wild bees. Based on 450 re-sightings, mean female flight distances ranged from 73 to 121 m and male distances from 59 to 100 m. These foraging distances suggest that as a rule of thumb, flower strips and nesting sites for supporting small solitary bees should be no further than 150 m apart.

Anthophila, body size, foraging distances, individual tagging, Megachilidae, solitary bees, urban garden

Wild bees are pollinators of high conservation concern. One reason for this derives from the relatively small spatial and temporal scale of their life cycles, habitat ranges, and nesting behaviour (Westrich 1996; Gathmann and Tscharntke 2002; Greenleaf et al. 2007; Franzén et al. 2009; Zurbuchen et al. 2010a; Wood et al. 2016), which makes them vulnerable to landscape fragmentation. Bees are central-place foragers, with females shuttling between foraging sites and nests to provide brood cells with pollen, nectar or oil, and the distance between these resources largely determines bees’ reproductive success (Zurbuchen et al. 2010b). The further nest and food sources are apart, the higher bees’ energetic and reproductive costs (Williams and Tepedino 2003; Zurbuchen et al. 2010b). Thus, in the European solitary species Hoplitis adunca and Chelostoma rapunculi (Megachilidae), the number of brood cells provisioned per time decreased by a third to almost half (31% or 46%) when foraging flight distances were experimentally increased by 200 or 500 m (Zurbuchen et al. 2010b). In the solitary Megachile rotundata, 74% fewer offspring were produced when flight distances increased by 150 m (Peterson and Roitberg 2006). Increased flight requirements reduce adult lifespan (Schmid-Hempel and Wolf 1988), and absences from the nest increase brood cell parasitism, as parasites enter the nest while the nest owner is away (Seidelmann 2006). Proximity of nesting and foraging sites is therefore crucial for the reproductive success of bees, and we need more data on foraging distances to predict the effects of habitat enhancements for conservation purposes (Nicholson et al. 2019).

Bee foraging distances have been investigated with a range of methods, including microsatellite DNA markers to determine to which colony a bumblebee worker belongs (Chapman et al. 2003; Knight et al. 2005), pollen analysis to check the content of pollen loads or brood cells for plants occurring at known distances (Williams and Tepedino 2003; Beil et al. 2008), and radio tracking for species large enough for carrying a transmitter (Carreck et al. 1999). The two most widely used methods are translocation experiments (e.g., Gathmann and Tscharntke 2002) and mark-recapture studies (e.g., Osborne et al. 2008; Wolf and Moritz 2008; Franzén et al. 2009; Zurbuchen et al. 2010a). In translocation experiments, bees are removed from their nest and released at increasing distances until no more returnees are recorded at the nesting sites. This is biologically highly different from a natural foraging flight in which a bee travels from, and returns to, its nest. Mark-recapture studies instead involve marking, releasing, and recapturing bees, but not transporting them (in darkened boxes) away from their nests.

All these approaches aim to find maximal flight distances, which are key to inferring body size/distance relationships. A linear regression model that included body length and maximum flight distance in 17 European solitary bees showed that distance roughly triples as body length doubles (Gathmann and Tscharntke 2002), with the smallest species studied being Chelostoma florisomne (7 to 11 mm), the largest the European carpenter bee Xylocopa violacea (20 to 30 mm). A non-linear regression analysis of the maximum distances of 62 species worldwide that regressed intertegular distance as a proxy for body size on distance found that larger bees had disproportionately larger foraging distances than smaller bees (Greenleaf et al. 2007).

Maximum flight distances can be treated as a species-level trait, i.e., the result of the averaged physiological and mechanical capacities of a species. In the present study, we instead focus on mean flight distances (which is not a species-level trait, but instead context-dependent), using a mark-release-re-sighting approach on large numbers of individuals of several species. Such data are needed to help conservation measures, such as the planting of flower strips or other resource stepping stones. Of 436 Central European species for which we compiled body sizes, 92% are between 4.5 and 13.5 mm long (Hofmann et al. 2019). We therefore selected six small species to quantify average flight distances in a flower-rich and nesting-site-rich botanic garden that harbours at least 106 species of wild bees (Hofmann et al. 2018). This provides independent data to compare to the flight distances of 150–600 m for 5.5 to 12 mm-long bees obtained in the above analysis in which bees were marked individually with ‘tip-ex’ or acrylic colour, transported to various release points, and the distance from the release site to the nest then measured (Gathmann and Tscharntke 2002).

To our knowledge, this is the largest tagging study of flight distances in solitary small bees in a flower-rich setting. The successful tracking of number and colour-coded tiny bees achieved in this study – ‘tracking’ because marked bees were not recaptured and hence not accidentally damaged or killed – was achieved through numerous search hours put in by students and citizen scientists in the botanical garden. In this way, we obtained 450 flight distances for six species of body lengths between 6 and 15 mm. These bees flew average distances of 75 to 125 m between their nests and their visited resources, with maximum distances up to seven times larger than mean distances (Table 2), supporting findings in other studies (Gathmann and Tscharntke 2002; Zurbuchen et al. 2010a, b) that did not use individual tagging but instead translocation experiments (e.g., Gathmann and Tscharntke 2002) or mark-recapture studies. Narrow foraging ranges thus appear to be the norm in solitary European bees, and even in the primitively eusocial Bombus terrestris, 40% of workers forage within a radius of 100 m around their nests (Wolf and Moritz 2008).

Bee foraging is highly context-dependent (e.g., Osborne et al. 2008; Pope and Jha 2018). For example, most Hoplitis adunca, a species in which both sexes prefer Echium flowers as pollen and nectar sources, were observed on exactly the various Echium plants in the garden. Given the context-dependence of bee foraging, a limitation of our study is that it is confined to one site. For the colour-tagged (rather than number-tagged) species, our flight distances also may be pseudo-replicated because the same bee could have been seen several times. Moreover, different plants in the garden are grouped in beds or by topic (Suppl. material 1: Figure S1), which must have influenced bee foraging patterns (but so would any resource distribution anywhere). Osmia cornuta is the only species investigated here with different-sized males and females, but the difference is small: Tables 1 and Suppl. material 2: Table S1.

Regardless of these limitations, our results support the correlation between body size and flight distance found with different methods in previous studies (Gathmann and Tscharntke 2002: 16 Central European species; Greenleaf et al. 2007: 62 species worldwide). This correlation implies that females of Central European bees, most of which are between 4.5 and 13.5 mm long (Hofmann et al. 2019), usually may not forage further than 125 to 150 meters from the nest (Gathmann and Tscharntke 2002: 150 to 600 m; our Table 2: 100 m). Despite the six or seven times larger distances that these bees are able to fly when forced to do so (Gathmann and Tscharntke 2002; Zurbuchen et al. 2010a, b), long flights between nests and floral resources have fitness costs in terms of lower offspring number and increased brood parasitism (Peterson and Roitberg 2006; Seidelmann 2006; Zurbuchen et al. 2010b). The persistence of populations therefore requires flower patches and nesting sites at suitable distances, for which we propose a rule-of-thumb of 150 m. This rule of thumb could be used by conservation practitioners planning urban greening measures. Implementing such simple habitat enhancements as flower strips with the appropriate spatial distribution, can greatly increase the connectivity of foraging sites and help bee conservation (Hofmann and Renner 2020).

We thank Carina Bader, Kerstin Behnke, Martin Gorgon, Jessica Grimm, Fernanda Herrera Mesías, Johannes Kirndorfer, Nona Kraus, Manuel Wagner, and Simone Well for support with bee tracking in the Botanical Garden, Constantin Zohner for statistical advice, and Sara Leonhardt and two anonymous reviewers for their comments on the manuscript.