Masked or yellow-faced bees of the genus Hylaeus (Colletidae) differ in their mode of pollen transportation from most other bees in that they ingest the pollen directly on the flowers and carry it back to the nest inside the crop located in the anterior half of the metasoma. Due to this hidden mode of pollen transportation, the examination of pollen collected by Hylaeus females requires the dissection of the metasoma. Although this method has never been applied in Europe, the great majority of the Central European Hylaeus species were supposed to be pollen generalists based on observations of flower visits. The microscopical analysis of pollen removed from 30 crops each of 36 Central European Hylaeus species revealed that the proportion of species exhibiting an exclusive or strong preference for pollen from a single plant taxon is much higher than hitherto assumed and that the current assumption of the genus Hylaeus to largely consist of pollen generalists is wrong. Nineteen of the 36 species examined are strictly or largely dependent on a single plant taxon for collecting pollen, such as Apiaceae (n = 11 species), Rosaceae (n = 3), Reseda (Resedaceae) (n = 2), Allium (Amaryllidaceae) (n = 1), Asteraceae (n = 1) and Melilotus (Fabaceae) (n = 1). The 36 Hylaeus species examined collected pollen from the flowers of 31 plant families, of which the Apiaceae and Rosaceae (particularly Potentilla and Rubus) were by far the most important contributing almost 60% to the pollen host spectrum of the entire genus. The comparison between pollen host spectrum and flower visiting records showed that the pollen generalists use the flowers of the Asteraceae as nectar rather than pollen sources, corroborating earlier findings that the digestion of Asteraceae pollen requires physiological adaptations to cope with its unfavourable or protective properties. In summary, the patterns of pollen host use by bees of the genus Hylaeus do not substantially differ from those of other Palaearctic bee taxa despite the masked bees’ unusual habit to ingest the pollen directly on the flowers and to transport it inside their body back to the nest.

Anthophila, Apiformes, Asteraceae paradox, Asteroideae, Carduoideae, oligolecty, polylecty

Bees are vegetarian wasps, whose larvae usually develop on a mixture of pollen and nectar within the brood cells of the nests built by the mother bees (Westrich 1989; Michener 2007). In most species, nesting females carry pollen collected on flowers back to the nest on the hind legs and/or on the underside of the metasoma (Westrich 1989; Michener 2007). Due to this external mode of pollen transportation, pollen is easily accessible for examination. In fact, extensive pollen analytical work starting with the seminal publications by Chambers (1968); Raw (1974); Westrich and Schmidt (1986, 1987) and Westrich (1989) and followed by numerous further investigations for example by Müller (1996, 2018); Michez et al. (2008); Müller and Kuhlmann (2008); Sedivy et al. (2008, 2013); Haider et al. (2014); Wood et al. (2016) or Wood and Roberts (2017) led to a fairly good knowledge of the pollen host preferences of large parts of the Central European bee fauna.

Bees of the genus Hylaeus – a cosmopolitan taxon of colletid bees comprising several hundred species worldwide (Ascher and Pickering 2020) – differ in their mode of pollen transportation from most other bees in that they ingest the pollen directly on the flowers and carry it back inside the metasomal crop to the nest, where it is regurgitated into the brood cells (Westrich 1989; Michener 2007). Due to this hidden mode of pollen transportation, pollen is accessible for examination only after dissection of the metasoma, a method that has never been applied for European species of this genus.

Based on field observations, all Central European Hylaeus species are currently assumed to be pollen generalists (“polylectic”) except for three species, which are most probably pollen specialists (“oligolectic”) on Allium (Amaryllidaceae), Reseda (Reseda) and Asteraceae, respectively (Scheuchl and Willner 2016; Westrich 2018; Wiesbauer 2020). However, reliable identification of Hylaeus in the field down to species level is strongly hampered by the small size and the uniform morphology of most Central European species, casting doubt on the field-based assumption that the vast majority of species is polylectic. Furthermore, as the spectrum of flowers exploited for nectar is often much wider than for pollen, observations of flower visits without careful differentiation between pollen and nectar uptake poorly reflect pollen host preferences and often conceal pollen specializations (Westrich and Schmidt 1987). In fact, the analysis of pollen remains in larval faeces of three North American Hylaeus species revealed that all three species collected pollen almost exclusively on Rosaceae in spite of long lists of flower visitation records comprising taxa belonging to numerous different plant families (Scott 1996).

In the present study, the pollen host preferences of 36 Central European Hylaeus species including four species restricted in their distribution to higher elevations in the Alps were analysed by microscopical analysis of pollen removed from the crops of collected females. Specifically, the following questions were addressed: i) What are the pollen host spectra of the Central European species? ii) Which plant taxa serve as the most important pollen hosts for the genus in Central Europe? iii) Are there differences between the pollen host spectrum of the genus as assessed in the present study and records of flower visits in the field?

The results of the present study show that the proportion of Central European Hylaeus species exhibiting an exclusive or strong preference for pollen from a single plant taxon is much higher than hitherto assumed and that the current assumption of the genus Hylaeus to largely consist of pollen generalists is wrong. Nineteen of the 36 Central European species examined are strictly or largely dependent on a single plant taxon for collecting pollen. For eleven of these species, flowers of the Apiaceae are the exclusive or strongly preferred hosts. The high significance of this plant family is also substantiated by the finding that the Apiaceae serve as pollen hosts for all Central European Hylaeus species with the exception of one polylectic species and three oligolectic species specialised on plant taxa other than the Apiaceae.

Phylogenetic inference is a powerful tool to reconstruct the evolution of pollen host preferences in bees (Müller 1996; Larkin et al. 2008; Sedivy et al. 2008, 2013; Haider et al. 2014). To date, no phylogeny of the genus Hylaeus including its Central European representatives is available, rendering any hypotheses on the evolution of pollen host use in this group of bees premature. Nevertheless, the results of the present study allow for some preliminary insights. First, species that show an exclusive or strong preference for Apiaceae occur in six out of the ten Central European subgenera; this finding suggests that the preference for Apiaceae might be an ancestral trait in the Palaearctic Hylaeus fauna or, alternatively, has independently evolved several times in the evolutionary history of the genus. Second, most species of the subgenus Paraprosopis are Apiaceae oligoleges, which suggests that the ancestor of the subgenus was specialised on Apiaceae. Third, the two morphologically similar and probably very closely related species Hylaeus pfankuchi and H. rinki (both belong to the subgenus Lamdopsis) have an almost identical pollen host spectrum with roughly 95% of the collected pollen originating from Potentilla, Rosa (both Rosaceae) and Apiaceae. Considering that these two Hylaeus species distinctly differ in their habitat choice with the former mainly occurring in wetlands with reed beds and the latter in forest clearings and along forest edges (Westrich 2018), the largely concordant pollen host choice likely has a genetic basis. The same might apply to two closely related species of the subgenus Dentigera, i.e. H. gredleri and H. kahri, which exhibit a strong preference for Apiaceae, as well as to the three species of the Hylaeus gibbus group, i.e. H. confusus, H. gibbus, H. incongruus, whose pollen host spectra are all dominated by Rosaceae and additionally include Apiaceae, Campanulaceae, Cistaceae, Hypericaceae and partly Fabaceae.

Flowers of 31 plant families serve as pollen hosts for the Central European Hylaeus species. With 33 families, the number of plant taxa exploited for pollen is similar in the western Palaearctic species of the related genus Colletes (Colletidae), and nearly 70% of the plant families used by the Hylaeus bees as pollen sources are also exploited by the Colletes bees (Müller and Kuhlmann 2008). Furthermore, there is no plant family in the pollen host spectrum of the genus Hylaeus, whose pollen is not collected by other short-tongued Central European bees, such as species of Andrena or Lasioglossum (Westrich 2018). Thus, the peculiar habit of Hylaeus bees to ingest the pollen directly on the flowers and to transport it back to the nest inside the crop does not translate into a pollen host spectrum different from other bee taxa.

The finding that 89% of the pollen collected by the Central European Hylaeus species originated from herbs and a further 9.6% from Rubus, which usually grows as a prostrate shrub, suggests that Hylaeus females restrict pollen harvesting mainly to the herbal layer. However, this finding might be biased since the females dissected for the present study were all netted by hand, which possibly resulted in an underrepresentation of specimens harvesting pollen in the shrub or tree layer. In fact, part of the pollen diet of Hylaeus communis in five European cities originated from trees (Casanelles-Abella et al. 2022).

About 93% of the plant taxa used by the Central European Hylaeus species as pollen hosts can also be exploited for nectar due to the easy access to the nectaries. In contrast, approximately 5% of the pollen hosts lack nectar or secrete nectar that is inaccessible to the Hylaeus bees. To compensate for this lack or inaccessibility of nectar, the females must visit other flowers to gain enough nectar for provisioning their brood cells, as is probably exemplified by the Asteraceae specialist Hylaeus nigritus and the pollen generalist H. dilatatus, for which flowers of Carduoideae (Asteraceae) are important pollen hosts. Although neither species is able to reach the nectaries at the base of the long-tubed Carduoideae flowers with their short proboscis, pollen of Carduoideae contributed 77.4% and 11.3% to the host plant spectra of H. nigritus and H. dilatatus, respectively. Interestingly, 25 out of 30 crop contents of H. nigritus contained a mixture of pollen from Carduoideae and Asteroideae, whereas only two contained solely Carduoideae pollen. Similarly, pollen of Carduoideae was recorded in 7 out of 30 crops in H. dilatatus but never constituted the only pollen type. This finding is likely explained by the necessity to combine mere pollen visits to the Carduoideae with visits to the Asteroideae or other plant taxa to obtain nectar.

The comparison between pollen host spectrum and flower visiting records revealed a striking discrepancy in the use of Asteraceae as host plants by the Central European Hylaeus species. After exclusion of the Asteraceae specialist Hylaeus nigritus, the percentage of Asteraceae pollen in the crop contents averaged only 1.1%, whereas more than 20% of all flower visiting females were observed on this plant family. The most likely explanation for this discrepancy is that the flowers of Asteraceae serve as nectar sources, but not or only marginally as pollen sources. This pattern of use of Asteraceae pollen by the Hylaeus bees supports recent findings that the pollen of this plant family possesses unfavourable or protective properties, which render its digestion difficult and necessitate physiological adaptations to successfully utilize it, resulting in a reduced ability to use alternative hosts (Müller and Kuhlmann 2008; Praz et al. 2008; Wood and Roberts 2018; Vanderplanck et al. 2020). This scenario – known as the Asteraceae paradox – neatly applies to the polylectic Hylaeus species, which hardly exploit Asteraceae for pollen, and to Hylaeus nigritus, which is specialised on Asteraceae. However, it does not apply to H. dilatatus, which is the only polylectic Hylaeus species in Central Europe that collects pollen to a considerable degree on Asteraceae. This species might have inherited the ability to successfully utilise Asteraceae pollen from an ancestor specialised on this plant family, as is possibly the case in the Colletes succinctus group, which comprises both Asteraceae oligoleges and polyleges that partly exploit Asteraceae for pollen (Müller and Kuhlmann 2008).

Bee diversity and abundance have considerably declined in large parts of Europe during the last decades (Nieto et al. 2014; Powney et al. 2019). Species of the genus Hylaeus are no exception: thirteen of the 40 Hylaeus species recorded for Switzerland and six of the 31 species occurring in Baden-Württemberg are red-listed (Westrich et al. 2000; Müller and Praz in prep.). The results of the present study enable the targeted improvement of the food supply for these species at risk. Moreover, given the high importance of Apiaceae, Rosaceae, Resedaceae and Fabaceae as pollen hosts, the promotion of summer flowering Apiaceae (particularly Daucus), of Potentilla and Rubus (both Rosaceae), of Reseda (Resedaceae) and of Melilotus (Fabaceae), for example by including them into wildflower seed mixtures for pollinators, benefits a large part of the Central European Hylaeus species.

Although species of the genus Hylaeus differ from most other bees by their unusual habit to ingest the pollen directly on the flowers and to transport it internally back to the nest, their patterns of pollen host use are comparable to those of numerous other Palaearctic bee taxa in that i) the genus comprises species that cover the whole spectrum of host plant associations ranging from narrow oligolecty to broad polylecty, ii) a similar set of pollen hosts is used as in many other short-tongued bees, such as Andrena, Colletes or Lasioglossum, and iii) Asteraceae are hardly exploited for pollen by the polylectic species.

The present study would not have been possible without the many bee specialists and curators of entomological collections who generously provided Hylaeus specimens for dissection: G. Artmann, M. Aubert, H. Baur (Naturhistorisches Museum Bern), D. Bénon, M. Bur, R. Burger, A. Freitag (Muséum Cantonal des Sciences Naturelles Lausanne), S. Gerber (Musée de la Nature Sion), M. Greef (ETH Zurich), S. Gurten, M. Haider, P. Heller, M. Herrmann, S. Klopfstein (Naturhistorisches Museum Basel), T. Kopf, J. Litman (Muséum d’Histoire Naturelle de Neuchâtel), R. Neumeyer, C. Praz, R. Prosi, A. Rey, A. Schanowski, F. Schmid, H.R. Schwenninger, C. Sedivy, B. Steinemann, F. von Mentlen, R. Wenger and T. Wood. K. Bieri (Biologisches Institut für Pollenanalyse Kehrsatz) helped with the identification of difficult pollen types. The Wildbienenkataster Baden-Württemberg (H.R. Schwenninger, A. Schanowski, R. Prosi) generously provided an excerpt of flower visiting data of 29 Hylaeus species from Baden-Württemberg. V. Mauss provided information on the anatomy and morphology of the crop in aculeate Hymenoptera. The Fachstelle für Naturschutz Zürich permitted the collection of a small number of Hylaeus specimens within a protected area. S. Falk, A. Haselböck, B. Jacobi, A. Krebs and N. Vereecken provided photos of flower visiting Hylaeus females. A private foundation financed the present study as part of the project “Mehr als Bienen” led by the Tierpark Goldau. D. Buresch and A. Mäder (Tierpark Goldau) accompanied the study with advice and support since its beginning in 2020. Numerous helpful suggestions and comments were made by E. Almeida, H. Dathe and J. Litman, who reviewed the manuscript.