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Research Article
Comparative ecology of two specialist bees: Dasypoda visnaga Rossi, 1790 and Dasypoda maura Pérez, 1895 (Hymenoptera, Melittidae)
expand article infoInsafe El Abdouni§, Patrick Lhomme§, Laila Hamroud§, Thomas Wood, Stefanie Christmann§, Pierre Rasmont, Denis Michez
‡ University of Mons, Mons, Belgium
§ International Center for Agricultural Research in the Dry Areas, Rabat, Morocco
Open Access

Abstract

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.

Keywords

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

Introduction

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).

Methods

Data collection

Historical data on distribution, floral choices and phenology were obtained from the database “Banque de données fauniques Gembloux Mons”. In total, we gathered information from 839 specimens of D. visnaga and 101 specimens of D. maura. These records come from different private and institutional collections (Berg, BMNH, Catania, CUI, DWB, Erfurt, FSAGX, Genève, GRUNWALD, ICC, IRSNB, Lausanne, LINSENMA, Livory A, MCN, Mendoça Li, University of Mentouri, MNHNP, Munich, NMV, OOLL, RNHL, Schwarz, UMons, UMO, UZMC, VERHOEFF, ZMA; 86% of the data) and literature (14% of data) (Suppl. material 1: Table S1).

We also collected additional specimens in Morocco to study the floral choices and some morphological traits related to the foraging behaviour of both species. Bees were collected using insect nets. They were then killed and separated for identification, trait measurement, and pollen analysis. Specimens are conserved in the collection of the University of Mons.

Phenological, morphological and ecological analyses

Phenological data were obtained from historical records and new Moroccan samples. Initially, records from all years were grouped by month and by country and we calculated the flight period of each species based on presence/absence of the species in each month. Then, we pooled all data for all countries to estimate the month(s) with the greatest number of observations for each species.

We considered the distance in millimetres between the two insertion points of the wings, the inter-tegular distance (ITD), as a proxy of body size (Cane 1987). We measured the length of the glossa and the prementum as a proxy of tongue length using a Facom 150 mm digital calliper (France, Morangis). These measurements were made from 31 specimens of D. visnaga (16 females and 15 males) and 39 specimens of D. maura (24 females and 15 males) from Morocco (Suppl. material 1: Table S2).

The floral utilization study of the two species of Dasypoda was based on floral visit observations and palynological analyses. The floral records represented 132 specimens, 87 specimens of D. visnaga (50 females and 37 males) and 45 specimens of D. maura (19 females and 26 males) (Suppl. material 1: Table S3).

Pollen analyses were based on the pollen loads removed from female scopa and the pollen balls sampled within the nest of both species. We analysed pollen from female scopa (three females of D. maura and seven for D. visnaga) and pollen balls (three pollen balls for D. maura and 10 for D. visnaga) from specimens newly collected in Morocco. We also used information from historical data presented by Michez et al. (2008), specifically 49 pollen loads of D. visnaga (from 34 localities) and 21 of D. maura (from 8 localities). Pollen was suspended in water on a microscope slide and allowed to rehydrate. The slide was then heated to evaporate the excess of water. Molten fuchsin jelly was added, and the slide was covered with a coverslip. Pollen grains were identified by light microscopy at a magnification of x400 using a reference collection of West Mediterranean plant species assembled from Iberia and North Africa (TJW pers. colln.). Identification to or below genus level in the family Asteraceae is highly challenging, and Scolymus-type pollen is characterised by typical Cichorieae shape at the tribal level, and to the group level by the diameter of the grains which measure 45–55 μm. This grain size included the related genera Cichorium, Helminthotheca, and Sonchus. Pollen grains representing less than 2% of the load were assumed to be contamination and neglected (Westrich and Schmidt 1986).

Foraging behaviour was evaluated by measuring visitation rate and time spent per flower (Pesenko et al. 1980; Akter et al. 2017). We examined the time of foraging on Scolymus hispanicus L. for the two species at the same site (45 females of D. visnaga and 44 females for D. maura). To quantify the visitation rate, we counted the number of flowers visited by each female (N = 18 females for each species) and the total time spent foraging. We then calculated the mean number of flowers visited per minute.

Investigation of the nesting architecture of both species was conducted in May (2019, 2020) and July (2019) in two locations in Rabat-Kenitra region. The nests of D. visnaga and D. maura were excavated in a site located at Douar Oulad Taleb near Maâmora forest (34.1243033°N, -6.5755842°W). The ground was sandy, bare, and exposed to the sun, with plants of Scolymus sp. 200 m away. A second nesting site of D. maura was investigated in Salé Al-Jadida (34.0226357°N, -6.7495343°W). This site was moderately vegetated with sandy and compacted soil. The flora included mostly Scolymus sp. and Carduus sp., but no Cichorium sp., Helminthotheca sp., or Sonchus sp. were recorded. One nest of each species was filled with liquid plaster and left 30 min until the plaster had solidified. This method allowed us to follow the tunnels and reconstruct the nest architecture (Tschinkel 2010). The other nests were excavated to sample pollen balls and larvae. After excavation, different parameters were measured: the distance between neighbouring nests, the width and the height of the tumulus, the length of tunnels, the number of cells and the depth of each cell.

Results

Phenology and distribution

Dasypoda visnaga is distributed in the north of Mediterranean Sea from Portugal to Turkey and in Maghreb (Morocco, Algeria, and Tunisia). Dasypoda maura is endemic to Northern Africa (Morocco and Algeria) (Fig. 1). In Morocco, D. maura is more widespread than D. visnaga, which is found only in coastal parts of the country while D. maura is also found in mountainous regions (Rif, Middle and High Atlas).

Records of both species show D. visnaga specimens were mainly collected in July (67%) whereas D. maura specimens were largely collected in May and June (90%) (Fig. 6). The beginning of the flight season of D. visnaga varies between countries, it starts in mid-April in Greece, in May in Morocco, Algeria, Tunisia, Spain and Portugal. It seems to start much later in France and Italy with specimens appearing in June. Dasypoda maura flies from April to July in Morocco and has been observed in July in Algeria (Fig. 2).

Figure 2. 

Temporal records of Dasypoda visnaga (light grey) and Dasypoda maura (dark grey).

Figure 3. 

Percentage of collected specimens per month for Dasypoda maura (dashed line, N = 110) and Dasypoda visnaga (solid line, N = 603) including data from all countries.

Morphological traits

Females of D. visnaga have the greatest ITD (3.60 ± 0.05 mm) followed by D. maura females (3.31 ± 0.02 mm) while the males of the two species have the smallest ITDs (D. visnaga: 3.18 ± 0.03 mm; D. maura: 3.19 ± 0.02 mm; Fig. 4A). We found a significant difference in ITD between females of both species and between males and females within and between species (Kruskal-Wallis, chi-squared = 40.55, df = 3, p = 8.122*10-9). No difference was found in ITD between males of both species (Wilcoxon rank-sum test, p = 1).

Figure 4. 

Morphological traits and estimated foraging distance of Dasypoda visnaga and D. maura A inter-tegulae distances B lengths of the proboscis. Box plots show the median and 25–75% percentiles. Whiskers show all data excluding outliers. Outliers (circles) are values being more than 1.5 times box length from upper and lower edge of respective box. The different letters indicate significant differences between treatments within experiments (Pairwise comparisons using Wilcoxon rank-sum test, p < 0.05).

Using a model estimating the foraging range based on body size (Greenleaf et al. 2007), we estimated the foraging distance of each species. The results showed that the estimated mean of foraging distance of D. visnaga females is 1.67 ± 0.03 km while D. maura females is 1.47 ± 0.01 km.

Tongue length was significantly different between species and sex (Kruskal-Wallis, chi-squared = 36.145, df = 3, p = 6.977*10-8). Dasypoda maura has the longest proboscis (female: 4.87 ± 0.019 mm; male: 4.66 ± 0.02 mm) while that of D. visnaga is shorter (female: 4.61 ± 0.07 mm; male 4.47 ± 0.04 mm, Fig. 4B).

Floral choices and foraging behaviour

Floral records of D. visnaga (50 females and 37 males) and D. maura (19 females and 26 males) obtained from historical data and new observations indicate that the most visited plant is almost exclusively Scolymus sp., except for males of D. maura who visit a greater diversity of host plants (Fig. 5). Males of D. maura visit a greater diversity of plants than males of D. visnaga. The alternative plants visited are Onopordum sp. (Asteraceae), Marrubium vulgare L. (Lamiaceae), Echinops spinosus L. (Asteraceae), and Scabiosa atropurpurea L. (Caprifoliaceae).

Figure 5. 

Floral choices of Dasypoda visnaga and D. maura based on historical and new Moroccan records. N is the number of records for each species and sex..

Palynological analyses revealed that pollen loads of D. maura contain only pollen of Scolymus-type. while 98% of loads from females of D. visnaga did the same. This result was confirmed by pollen analysis of pollen balls found in the nest in Morocco as all pollen balls analysed consisted of Scolymus-type pollen. Given the absence of related plant genera that produce this pollen type at this study site (see Methods), Scolymus plants are highly likely to be the sole pollen source at this locality.

The mean time spent on a flower of Scolymus hispanicus L. by D. visnaga (4.17 s) and D. maura (3.83 s) were similar (Wilcoxon rank-sum test, p = 0.25) (Fig. 6B). However, D. visnaga visited a higher number of flowers per minute (13 flower/min) than D. maura (9 flowers/min) (Fig. 6A).

Figure 6. 

A frequency of floral visits B average flower visit duration between Dasypoda maura and Dasypoda visnaga. The different letters indicate significant differences between species (A student t-test, p < 0.05 B Wilcoxon rank-sum test, p > 0.05).

Nest architecture

Females of D. visnaga construct their nests in sandy and non-compacted soil making a heap of sand above the nest entrance called a tumulus (Fig. 7B). This tumulus is built from soil displaced by the female during nest excavation. The diameter of the tumulus ranges from 7 to 10 cm (8.6 ± 1.07 cm) and the height ranges from 1 to 4 cm (2.89 ± 1.34 cm). The main burrow has a diameter of 10 mm, it is oblique on 25 cm and at an angle of 45° then it becomes vertical. The main burrow reaches 80 cm in length (Fig. 7E). The female constructs the brood cells connected to the main burrow by lateral burrows located at different depths. Cells were filled with a spherical pollen ball (without a tripod) with the egg placed on the top (Fig. 7E). After laying the egg, the female closes the cell with an earthen plug and tightly fills the lateral burrow with soil.

Figure 7. 

A, B nesting sites C, D nest entrances E, F nest architecture showing main galleries, hypothetical cells, and pollen balls G, H larva with pollen balls. Right side: Dasypoda maura, left side: Dasypoda visnaga.

Nest entrances of D. maura (Fig. 7A) were difficult to find because they do not possess conspicuous tumuli like those of D. visnaga (Fig. 7D) and were usually found below vegetation cover. The diameter of the flat nest tumuli ranges from 12 to 16 cm (13.5 ± 1.17 cm). The distance between nests within an aggregation ranges from 32 cm to 170 cm. The females build their nests also in sandy soil with a low proportion of clay. The main burrow has a diameter of 8 mm and a length of 80 cm. The brood cells are also connected to the main burrow by lateral ones located at different depths and each cell contains a pollen ball with a basal tripod (Fig. 7F). The egg was also laid on the top of the pollen ball.

Discussion

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).

Conclusion

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.

Acknowledgements

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)”.

References

  • Bartomeus I, Ascher JS, Gibbs J, Danforth BN, Wagner DL, Hedtke SM, Winfree R (2013) Historical changes in northeastern US bee pollinators related to shared ecological traits. Proceedings of the National Academy of Sciences of the United States of America 110: 4656–4660. https://doi.org/10.1073/pnas.1218503110
  • Biesmeijer JC, Roberts SPM, Reemer M, Ohlemüller R, Edwards M, Peeters T, Schaffers AP, Potts SG, Kleukers R, Thomas CD, Settele J, Kunin WE (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313: 351–354. https://doi.org/10.1126/science.1127863
  • Burkle LA, Marlin JC, Knight TM (2013) Plant-pollinator interactions over 120 years: Loss of species, co-occurrence, and function. Science 340: 1611–1615. https://doi.org/10.1126/science.1232728
  • Cane JH (1987) Estimation of bee size using intertegular span (Apoidea). Journal of the Kansas Entomological Society 60: 145–147.
  • Celary W (2002) The ground-nesting solitary bee, Dasypoda thoracica BAER, 1853 (Hymenoptera: Apoidea: Melittidae) and its life history. Folia Biologica 50: 191–198.
  • Christmann S (2019) Do we realize the full impact of pollinator loss on other ecosystem services and the challenges for any restoration in terrestrial areas? Restoration Ecology 27: 720–725. https://doi.org/10.1111/rec.12950
  • Danforth BN, Minckley RL, Neff JL, Fawcett F (2019) The Solitary Bees: Biology, Evolution, Conservation. Princeton University Press, Princeton, 472 pp. https://doi.org/10.1515/9780691189321
  • Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined Stress from parasites, pesticides, and lack of flowers. Science 347(6229): e1255957. https://doi.org/10.1126/science.1255957
  • Kleijn D, Winfree R, Bartomeus I, Carvalheiro LG, Henry M, Isaacs R, Klein AM, Kremen C, M’Gonigle LK, Rader R, Ricketts TH, Williams NM, Lee Adamson N, Ascher JS, Báldi A, Batáry P, Benjamin F, Biesmeijer JC, Blitzer EJ, Bommarco R, Brand MR, Bretagnolle V, Button L, Cariveau DP, Chifflet R, Colville JF, Danforth BN, Elle E, Garratt MPD, Herzog F, Holzschuh A, Howlett BG, Jauker F, Jha S, Knop E, Krewenka KM, Le Féon V, Mandelik Y, May EA, Park MG, Pisanty G, Reemer M, Riedinger V, Rollin O, Rundlöf M, Sardiñas HS, Scheper J, Sciligo AR, Smith HG, Steffan-Dewenter I, Thorp R, Tscharntke T, Verhulst J, Viana BF, Vaissière BE, Veldtman R, Westphal C, Potts SG (2015) Delivery of crop pollination services is an insufficient argument for wild pollinator conservation. Nature Communications 6: e7414. https://doi.org/10.1038/ncomms8414
  • Klumpers SGT, Stang M, Klinkhamer PG (2019) Foraging efficiency and size matching in a plant-pollinator community: the importance of sugar content and tongue length. Ecology Letters 22: 469–479. https://doi.org/10.1111/ele.13204
  • Levermann E-M, Bischoff I, Wagner T (2000) Species-specific foraging strategies of the syntopical and synchronous bees Panurgus calcaratus (Scopoli, 1763) and Dasypoda hirtipes (Fabricius), 1793 (Hymenoptera: Apidae). Beiträge zur Entomologie 50: 179–191. https://doi.org/10.21248/contrib.entomol.50.1.179-191
  • Lhomme P, Michez D, Christmann S, Scheuchl E, El Abdouni I, Hamroud L, Ihsane O, Sentil A, Smaili MC, Schwarz M, Dathe HH, Straka J, Pauly A, Schmid-Egger C, Patiny S, Terzo M, Müller A, Praz C, Risch S, Kasparek M, Kuhlmann M, Wood TJ, Bogusch P, Ascher J, Rasmont P (2020) The wild bees (Hymenoptera: Apoidea) of Morocco. Zootaxa 4892(1): 001–159. https://doi.org/10.11646/zootaxa.4892.1.1
  • Loonstra FAJ (2010) Observaties van en onderzoek aan nesten en ontwikkeling van Dasypoda hirtipes en Panurgus calcaratus. Hymeno Varia 1: 19–23.
  • Malyshev SI (1927) The nesting habits of Dasypoda Latr. (Hymenoptera, Apoidea). Trudy Leningradskogo obshchestva estestvoispytatelei (Leningrad) 57(2): 123–146.
  • Malyshev SI (1931) Recommendation for Collecting and Studying the Nests of Bees and Some Other Hymenopterans. Leningrad, Academy of Sciences of the USSR, 81 pp.
  • Malyshev SI (1936) The nesting habits of solitary bees. A comparative study. Eos (Madrid) 11(3): 201–309.
  • Michener CD (2007) The Bees of the World (2nd edn.). The Johna Hopkins University Press, Baltimore, 894 pp.
  • Michez D, Terzo M, Rasmont P (2004a) Phylogénie, biogéographie et choix floraux des abeilles oligolectiques du genre Dasypoda Latreille, 1802 (Hymenoptera: Apoidea: Melittidae). Annales de la Société Entomologique de France 40: 421–435. https://doi.org/10.1080/00379271.2004.10697431
  • Michez D, Terzo M, Rasmont P (2004b) Révision des espèces ouest-paléarctiques du genre Dasypoda Latreille, 1980 (Hymenoptera, Apoidea, Melittidae). Linzer biologische Beitrage 36: 847–900.
  • Michez D, Patiny S, Danforth BN (2009) Phylogeny of the bee family Melittidae (Hymenoptera: Anthophila) based on combined molecular and morphological data. Systematic Entomology 34: 574–597. https://doi.org/10.1111/j.1365-3113.2009.00479.x
  • Michez D, Sébastien P, Pierre R, Kim T, Nicolas JV (2008) Phylogeny and host-plant evolution in Melittidae (Hymenoptera : Apoidea). Apidologie 39: 146–162. https://doi.org/10.1051/apido:2007048
  • Müller A, Diener S, Schnyder S, Stutz K, Sedivy C, Dorn S (2006) Quantitative pollen requirements of solitary bees: Implications for bee conservation and the evolution of bee-flower relationships. Biological Conservation 130: 604–615. https://doi.org/10.1016/j.biocon.2006.01.023
  • Müller H (1884) Ein Beitrag zur Lebensgeschichte der Dasypoda hirtipes. Verhandlungen des Naturhistorischen Vereins der Preussischen Rheinlande und Westfalens 41: 1–51.
  • Nieto A, Roberts SPM, Kemp J, Rasmont P, Kuhlmann M, García Criado M, Biesmeijer JC, Bogusch P, Dathe HH, De la Rúa P, De Meulemeester T, Dehon M, Dewulf A, Ortiz-Sánchez FJ, Lhomme P, Pauly A, Potts SG, Praz C, Quaranta M, Radchenko V, Scheuchl E, Smit J, Straka J, Terzo M, Tomozii B, Window J, Michez D (2014) European Red List of Bees. Luxembourg: Publication Office of the European Union. https://doi.org/10.2779/77003
  • Osborne JL, Andrew P, Carreck NL, Swain JL, Knight ME, Goulson D, Hale RJ, Sanderson RA (2008) Bumblebee flight distances in relation to the forage landscape. Journal of Animal Ecology 77: 406–415. https://doi.org/10.1111/j.1365-2656.2007.01333.x
  • De Palma A, Kuhlmann M, Roberts SPM, Potts SG, Börger L, Hudson LN, Lysenko I, Newbold T, Purvis A (2015) Ecological traits affect the sensitivity of bees to land-use pressures in European agricultural landscapes. Journal of Applied Ecology 52: 1567–1577. https://doi.org/10.1111/1365-2664.12524
  • Pesenko YA, Radchenko VG, Kaygorodova MS (1980) Ecology of pollination in Strigosella grandiflora and Erysimum badghysi (Brassicaceae) by bees (Hymenoptera, Apoidea) in Badkhyz: Estimation of the pressure of competitive relationships. Entomological Review 59: 58–73.
  • Potts SG, Imperatriz-Fonseca V, Ngo HT, Aizen MA, Biesmeijer JC, Breeze TD, Dicks LV, Garibaldi LA, Hill R, Settele J, Vanbergen AJ (2016) Safeguarding pollinators and their values to human well-being. Nature 540: 220–229. https://doi.org/10.1038/nature20588
  • Potts SG, Vulliamy B, Dafni A, Ne’eman G, Willmer P (2003) Linking bees and flowers: How do floral communities structure pollinator communities? Ecology 84: 2628–2642. https://doi.org/10.1890/02-0136
  • Potts SG, Betsy V, Roberts S, O’Tootle C, Dafni A, Ne’man G, Willmer P (2005) Role of nesting resources in organizing diverse bee communities in Mediterranean landscape. Ecological Entomology 30: 78–85. https://doi.org/10.1111/j.0307-6946.2005.00662.x
  • Powney GD, Carvell C, Edwards M, Morris RKA, Roy HE, Woodcock BA, Isaac NJB (2019) Widespread losses of pollinating insects in Britain. Nature Communications 10: 1–6. https://doi.org/10.1038/s41467-019-08974-9
  • Radchenko VG (1988) Nesting of Dasypoda braccata Eversm. (Hymenoptera, Melitidae) in the southwestern Ukraine. Entomologicheskoye Obozreniye 67: 302–320.
  • Radchenko VG (1996) Evolution of nest building in bees (Hymenoptera, Apoidea). Entomological Review 75: 20–32.
  • Radchenko VG (2017) A new bee species of the genus Dasypoda Latreille (Hymenoptera, Apoidea) from Portugal with comparative remarks on the subgenus Heterodasypoda Michez. Zootaxa 4350: 164–176. https://doi.org/10.11646/zootaxa.4350.1.10
  • Radchenko VG, Pesenko YA (1989) A key to the bees of the genus Dasypoda Latreille (Hymenoptera, Melittidae) of the European part of the USSR, with a designation of lectotypes. Trudy Zoologicheskogo Instituta, Akademiya Nauk SSSR 188: 114–121.
  • Radchenko VG, Pesenko YA (1994) Biology of bees (Hymenoptera: Apoidea). Zoological Institute, Russian Academy of Sciences, St. Petersburg, 350 pp.
  • Radchenko VG, Ghisbain G, Michez D (2019) Redescription of three rare species of Dasypoda bees with first description of D. iberica and D. tibialis females (Hymenoptera, Apoidea, Melittidae). Zootaxa 4700: 326–344. https://doi.org/10.11646/zootaxa.4700.3.2
  • Razo-León AE, Vásquez-Bolaños M, Muñoz-Urias A, Huerta-Martínez FM (2018) Changes in bee community structure (Hymenoptera, Apoidea) under three different land-use conditions. Journal of Hymenoptera Research 66: 23–38. https://doi.org/10.3897/jhr.66.27367
  • Roswell M, Dushoff J, Winfree R (2019) Male and female bees show large differences in floral preference. PLoS ONE 14: e0214909. https://doi.org/10.1101/432518
  • Sakagami SF, Michener CD (1962) The Nest Architecture of the Sweat Bees (Halictinae). A comparative study of behavior. Lawrence, University of Kansas Press, Lawrence, 135 pp.
  • Scheper J, Reemer M, Van Kats R, Ozinga WA, Van Der Linden GTJ, Schaminée JHJ, Siepel H, Kleijn D (2014) Museum specimens reveal loss of pollen host plants as key factor driving wild bee decline in the Netherlands. Proceedings of the National Academy of Sciences of the United States of America 111: 17552–17557. https://doi.org/10.1073/pnas.1412973111
  • Vereecken N, Toffin E, Michez D (2006) Observations relatives à la biologie et la nidification de quelques abeilles sauvages psammophiles d’intérêt en Wallonie. Parcs & Reserves 61: 12–20.
  • Westrich P, Schmidt K (1986) Methoden und Anwendungsgebiete der Pollenanalyse bei Wildbienen (Hymenoptera, Apoidea). Linzer Biologische Beiträge 18: 341–360. https://doi.org/10.1051/apido:19870209
  • Williams NM, Crone EE, Roulston TH, Minckley RL, Packer L, Potts SG (2010) Ecological and life-history traits predict bee species responses to environmental disturbances. Biological Conservation 143: 2280–2291. https://doi.org/10.1016/j.biocon.2010.03.024
  • Zurbuchen A, Landert L, Klaiber J, Müller A, Hein S, Dorn S (2010) Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances. Biological Conservation 143: 669–676. https://doi.org/10.1016/j.biocon.2009.12.003

Supplementary material

Supplementary material 1 

Tables S1–S3

Insafe El Abdouni, Patrick Lhomme, Laila Hamroud, Thomas Wood, Stefanie Christmann, Pierre Rasmont, Denis Michez

Data type: Occurences, morphological traits, floral preferences

Explanation note: Table S1: distribution data of Dasypoda visnaga and Dasypoda maura; Table S2: morphological trait and forging distance measurement; Table S3: floral preferences of Dasypoda visnaga and Dasypoda maura.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
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