Many wild bee species are declining globally. To design efficient mitigation strategies to slow down or reverse these trends, we urgently need to better understand their basic ecological requirements. In this context, we studied two specialist species for which ecological data are scarce: Dasypoda visnaga and Dasypoda maura. We provide for the first-time detailed information on their phenologies, morphological traits, floral preferences, and nesting behaviours based on historical data and new samples from Morocco. The flight season of both species extends from late spring to late summer but D. maura emerges earlier than D. visnaga. Though the two species show different morphological traits, palynological analyses show that D. visnaga and D. maura females collect almost exclusively pollen from Scolymus sp. (Asteraceae). Concerning their nesting behaviour, D. visnaga seems to be more gregarious than D. maura. Both species build nests in sandy soil that can reach a depth of 80 cm. These ecological observations show that the differences between D. visnaga and D. maura are minor with regards to habitat requirements.

Conservation, floral preferences, habitat requirements, nesting behaviour, phenology, Scolymus

Worldwide declines in wild bee populations have been reported over the past two decades (Biesmeijer et al. 2006; Burkle et al. 2013; Nieto et al. 2014; Kleijn et al. 2015; Potts et al. 2016; Christmann 2019; Powney et al. 2019). To contain these declines, there is an urgent need to better understand their specific foraging and nesting requirements in order to design efficient mitigation strategies (Müller et al. 2006). Host plant and nesting resource (i.e. materials and substrates) availability are the two principal components driving the structure of wild bee communities (Potts et al. 2003, 2005; Goulson et al. 2015; Razo-León et al. 2018).

Regarding their floral choices, wild bees are usually described as specialists or generalists depending on their foraging strategies. Specialist (or oligolectic) bees exhibit a high fidelity for particular plant taxa of the same botanical family while generalist (or polylectic) bees forage on a wide range of plants from multiple botanical families (Rasmussen et al. 2020). These diverse foraging behaviours influence the composition of bee communities (Scheper et al. 2014) and their conservation. Specialist bees are more affected than generalists by disturbances such as agricultural intensification (Williams et al. 2010) as they are not able to switch to alternative plant resources.

Bees also show a great diversity of nesting behaviours. The majority are ground nesters but some species nest above ground in various substrates such as hollow or pithy stems or abandoned cavities in dead wood or build their nests on open surfaces (Radchenko and Pesenko 1994; Danforth et al. 2019). They can also use various material to build their cells such as mud, pebbles, resin, flower petals, plant leaves, plant hairs, floral oils or secreted building materials (Radchenko 1996; Cane et al. 2007; Danforth et al. 2019). In addition, there are also parasitic (e.g. cuckoo bees) species, which exploit the nest built by their bee host and lay their eggs on the pollen provisions (Michener 2007). They can even exploit the social system of their host in the case of socially parasitic bees (Lhomme and Hines 2019). Within ground-nesting bees, species can show specific nesting site requirements (e.g. soil texture / moisture / compaction, vegetation cover, exposed bare ground) (Potts and Willmer 1997; Sardiñas and Kremen 2014) or nest architecture (e.g. variation in depth and relative position of cells). Nesting resource availability and soil characteristics can therefore greatly affect the composition of bee communities, and 40% of the variation in species abundance pattern can be explained by the availability of nesting resources (Potts et al. 2005). Unfortunately, disturbances like habitat fragmentation, agricultural intensification, pesticide use and tillage can have a negative impact on nesting resources (Williams et al. 2010).

Among the ~20 000 described bee species, melittid bees constitute one of the smallest families (201 species; Michez et al. 2009; Danforth et al. 2013). As they are relatively rare and localised, data on their ecology are scarce. Within this bee family, the genus Dasypoda comprises 39 described species (Michez et al. 2004a; Radchenko 2016, 2017; Radchenko et al. 2019). Among them, nine species are recorded in Morocco (Lhomme et al. 2020). Dasypoda species are predominantly oligolectic, with the exception of some species such as Dasypoda crassicornis Friese which are known to be polylectic. The subgenera Dasypoda s. str. and Megadasypoda forage on Asteraceae and Dipsacaceae respectively while Heterodasypoda and Microdasypoda subgenera visit mainly Cistaceae and Malvaceae (Michez et al. 2004b). Regarding their nesting behaviour, Dasypoda species are known to nest in the ground based on studies of three species: D. argentata Panzer (as D. thoracica Baer) (Celary 2002), D. braccata Eversmann (Radchenko 1988), and D. hirtipes Fabricius (Müller 1884; Vereecken et al. 2006; Loonstra 2010). Based on the information gathered from these species, we know that after mating, Dasypoda females initiate nest construction in sandy soil and then start to collect pollen. They place pollen balls in brood cells and lay an egg on the top. The larvae feed on the pollen ball and do not spin a cocoon. The nests are generally deep and can exceed more than 90 cm in depth (Celary 2002). Some species like D. hirtipes build their cells near the main gallery and make tripod-like structures below the pollen balls to reduce contact between the provisions and the cell wall (Müller 1884; Vereecken et al. 2006).

This paper aims to increase our knowledge concerning the ecology of the genus Dasypoda focusing on two species observed in Morocco, Dasypoda maura Pérez 1895 and Dasypoda visnaga Rossi 1790 (Fig. 1). The floral choices and nesting behaviour of these species are poorly documented, so this study aims to describe their phenologies, distribution, host plant preferences, and nesting ecology.

Figure 1. 

A Dasypoda visnaga female. Photo by Patrick Lhomme (2020) B Dasypoda maura female foraging on Scolymus hispanicus. Photo by Insafe El Abdouni (2020) C geographical distribution of the two species (pink circles = records of Dasypoda visnaga; black circles = records of Dasypoda maura).

The present study revealed that the two studied Dasypoda species have similar ecological requirements with slight differences. Dasypoda visnaga is found in most Mediterranean countries, especially in coastal areas. This distribution is probably related to the type of soil as D. visnaga nests in non-compacted sand, and its main host plant Scolymus hispanicus is often found in coastal areas. Dasypoda maura is additionally found inland in Morocco. The soil where D. maura nests can be much more compact than the soil where nests of D. visnaga were observed. Phenological records in Morocco and other countries showed that D. visnaga and D. maura are mainly active during late spring and summer (April-August). This period coincides with the flowering of Scolymus plants. This suggests the presence of one generation per year like others species of Dasypoda (Radchenko and Pesenko 1989; Vereecken et al. 2006).

Morphological data showed that the females of D. visnaga have a larger body size than D. maura. Following Greenleaf et al. (2007) model, the estimated foraging distance for both species should be large. This distance is close to other large species like Bombus terrestris Linnaeus (1500 m) (Osborne et al. 2008) or Hoplitis adunca Panzer (1400 m) (Zurbuchen et al. 2010). Consequently, Dasypoda species could be less sensitive to disturbances like habitat destruction (De Palma et al. 2015). A slight trend for small species to be more sensitive to land disturbance has been found (Bartomeus et al. 2017), but other studies have shown a positive correlation between body size and sensitivity to agricultural land use (Bartomeus et al. 2013).

Females of the two species have a different tongue length but the same foraging duration on flowers of Scolymus. The time spent per flower for D. visnaga and D. maura (4.2 s and 3.8 s respectively) is higher than for D. hirtipes (0.7 s) (Levermann et al. 2000). According to Klumpers et al. (2019), the interaction between the length of a proboscis and the depth of corolla affects the handling time. Insects with a proboscis shorter than nectar tubes spend more time foraging per flower on these flowers and are consequently a less efficient. In this study, the two bee species forage on the same plant species so the time spent foraging does not seem to be affected by tongue length. However we used a different metric and did not investigate the handling time as described by Klumpers et al. (2019) which is the time that an insect takes to extend its proboscis and extract the nectar. Records from historical data and our observations show that D. visnaga and D. maura have similar floral preferences. They forage mostly on Asteraceae family confirming the position of Michez et al. (2008). Pollen analyses revealed that both species are strict oligoleges of Asteraceae, and though it cannot be proved definitively with light microscopy, females are highly likely to provision their offspring with pollen of Scolymus plants exclusively, thus making them narrow oligoleges. The comparison between male and female choices shows the presence of large differences in floral choices that are known to exist between different bee sexes (Roswell et al. 2019).

Dasypoda maura and D. visnaga seem to have nesting behaviour and nest architecture similar to the other Dasypoda nests described so far. After emergence and mating, females of D. visnaga start to build their nests in sandy soil, similar observations were made for Dasypoda hirtipes (Vereecken et al. 2006) and Dasypoda argentata (Celary 2002) whereas, Dasypoda braccata prefers soil with a high clay content (Radchenko 1988). Females first excavate an oblique burrow for about 25–30 cm. Then, the burrow changes direction and females start to construct cells where they put pollen balls. Pollen balls made by D. visnaga do not possess any tripod and were put directly on the soil at the bottom of the cells, which do not have the additional lining that characteristic of many other ground-nesting bees (Fig. 7E) while D. maura pollen possess tripods (Fig. 7F), like D. hirtipes, another species from the same subgenus (Müller 1884; Vereecken et al. 2006).

This study is the first to compare ecological aspects of two species of Dasypoda bees. Both studied species are oligolectic and share many ecological traits. They have very restricted floral preferences and nesting requirements. Future surveys should be performed to better understand their ecology and assess if conservation strategies are needed. The two species were found in agricultural landscape, so these strategies should consider the role of farmers. They should be informed and trained to recognise the bee nests and their host plant to protect them in local areas.

This research was funded by the Federal German Ministry for the Environment, Nature Conservation and Nuclear Safety (BMU) through the International Climate Initiative (IKI). It was also partly supported by the “Fonds de la Recherche Scientifique – FNRS”, the “Research Foundation of Flanders – FWO” under EOS Project named CLIPS (n°3094785) and by the “Académie de Recherche et d’Enseignement Supérieur (ARES)”.