Research Article |
Corresponding author: Petr Bogusch ( bogusch.petr@gmail.com ) Academic editor: Jack Neff
© 2020 Petr Bogusch, Lucie Hlaváčková, Libor Petr, Jordi Bosch.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Bogusch P, Hlaváčková L, Petr L, Bosch J (2020) Nest structure, pollen utilization and parasites associated with two west-Mediterranean bees (Hymenoptera, Apiformes, Megachilidae) nesting in empty snail shells. Journal of Hymenoptera Research 76: 113-125. https://doi.org/10.3897/jhr.76.49579
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Around thirty species of European solitary bee species in the family Megachilidae nest in empty gastropod shells. We surveyed this group of bees in semi-natural sites adjacent to almond orchards near Lleida (north-eastern Spain) and collected 35 Hoplitis fertoni and 58 Osmia ferruginea nests in shells of six snail species. We describe the nest structure and report the identity of pollens collected by the two bee species. Both species adjust the number of brood cells to the size of the shell and occasionally build intercalary (empty) cells. H. fertoni uses clay and O. ferruginea chewed plant leaves for building cell partitions and nest plugs. Most nests of both species were built in Sphincterochila candidissima shells. Analysis of the pollen of selected nests confirmed that H. fertoni is oligolectic on Boraginaceae (in our study all pollen was from Lithodora fruticosa) and O. ferruginea is a polylectic species (collecting mostly pollen from Cistaceae, Fabaceae, and Lamiaceae in our study area). Nests of H. fertoni were parasitized by five species, the golden wasp Chrysura hybrida, the cuckoo bee Dioxys moesta, the velvet ants Stenomutilla collaris and Stenomutilla hotentotta, and the bee-fly Anthrax aethiops; nests of O. ferruginea were parasitized by the sapygid wasp Sapyga quinquepunctata and A. aethiops. Except for C. hybrida these are newly recorded host-parasite associations. Our results confirm previous information and bring new findings on the ecology of both species.
Spain, Lleida, Hoplitis fertoni, Osmia ferruginea, parasitoid, cleptoparasite, pollen specialization
Bees (Anthophila/Apiformes) are a very speciose clade of Hymenoptera, with more than 20,000 species worldwide (
Hoplitis fertoni occurs in North Africa, Spain, Portugal, and Sicily, and may be locally abundant. It builds its nests in shells of large snail species (such as Eobania, Otala and Theba), and uses mud to build brood cell partitions and to close the nest (
Osmia ferruginea occurs in all countries around the Mediterranean and may be locally common in the West-Mediterranean region (
Here, we describe the nest structure of Hoplitis fertoni and Osmia ferruginea, and report on the snail shells used and the pollens collected by these two species. We also report on several parasitoids and nest cleptoparasites reared from the collected nests. We discuss our results in relation to previous information available for these two species (
In March 2019 we collected more than 500 large gastropod shells (the size of semiadult Cernuella virgata, 8 mm, or bigger) in 10 semi-natural sites with high shell availability around almond orchards near Lleida. We also collected 434 shells in three additional localities in which shell availability was lower. Some of the shells contained Hoplitis fertoni nests built in the previous year (with cocoons). Other shells contained fresh Osmia ferruginea nests (with provisions and eggs/larvae).
Hoplitis fertoni nests were dissected 0–8 days after collection. The number of brood cells, their shape and positions within the shell and the number of larvae, pupae and adults were recorded. Some remnants of pollen provisions were collected and placed inside plastic micro-tubes for later identification. Some O. ferruginea nests were also dissected 0–8 days after collection. The rest were dissected at biweekly intervals until May 11th, when all nests contained mature larvae in cocoons (prepupae). All brood was kept under laboratory conditions until adult eclosion which occurred by September the same year. The cocoons were opened in September 2019, when all bees and their parasites developed into adults and were alive inside the cocoons, two specimens of the brood parasite Sapyga quinquepunctata spontaneously hatched and left the cocoons a few days before we opened them.
Pollen samples were prepared using a standard acetolysis method (
Photos of shells containing nests, closing plugs, and dissected nests were taken with a digital camera Nikon Coolpix B500. Photos of larvae, brood cells, and nest details were taken with a digital camera Canon EOS 550 and a macro-objective equipped with LED goose-neck light. Final figures were created from multiple level-photos stacked by Zerene Stacker software. We drew figures of nest structure using pen-drawing and colouring in Adobe Photoshop. Photos of pollen grains were taken under a light microscope Delphi X-Observer DX 2153-PLi with a camera Moticam 5+ and software for photo analysis.
We collected 35 gastropod shells with nests of H. fertoni in three of the 13 localities surveyed. All of the localities were situated in dry hilly region. All shells were found on the ground surface and were not hidden. The closing plug was made of soil of light-brownish or greyish colour (Fig.
Structure of Hoplitis fertoni (A, D) and Osmia ferruginea (B, C, E) nests A shell of Sphincterochila candidissima with nest of H. fertoni B shell of S. candidissima with nest of O. ferruginea C larva of O. ferruginea on pollen-nectar provision D nest structure of H. fertoni E nest structure of O. ferruginea. Photos and drawings by P. Bogusch.
The majority (26, 74.3%) of the nests were built in shells of Sphincterochila candidissima. Other snail species used were Eobania vermiculata (4, 11.4%), Cernuella sp. (3, 8.6%) and Otala lactea (1, 2.9%). The 35 nests collected contained 217 brood cells (mean ± SD: 6.2 ± 2.24; range: 2–10 brood cells per nest). The nests in S. candidissima shells contained 4–9 brood cells (mean 6.4, median 7), and those in E. vermiculata shells 5–10 brood cells (mean 5.8, median 6). Nests in the smaller Cernuella sp. shells contained fewer cells (range 2–3, mean 2.3, median 2).
Altogether 58 (26.7%) brood cells contained dead, dry or mouldy contents. Of the remaining brood cells, 126 contained pupae or adults of H. fertoni, and 33 were parasitized (25.8% of brood cells containing live insects). The golden wasp Chrysura hybrida (Chrysididae) was the most common parasitoid (21 cells in 14 nests). Cells parasitized by C. hybrida were recognizable by the presence of a semi-transparent brownish cocoon with a whitish spot within the thicker brownish cocoon of H. fertoni. We also found five nests parasitized by the velvet ant Stenomutilla collaris (seven cells) and one nest by Stenomutilla hotentotta (one cell) (Mutillidae). Velvet ants pupated and became adults by late spring (late May – June). Stenomutilla cocoons were very similar to those of C. hybrida but harder and darker and did not have whitish marks. We also found three nests parasitized by the cuckoo bee Dioxys moesta (Megachilidae) (one cell per nest). The cocoons of this species were composed of a single whitish layer sparsely covered with dark brownish faecal particles. Pupation and adult eclosion occurred more or less at the same time as in H. fertoni. Finally, we found one nest with one cell parasitized by the bee-fly Anthrax aethiops (Bombyliidae). The structure of all nests is illustrated in Fig.
We analysed pollen samples (remnants of unconsumed provisions) from six nests from two localities (S35 and S37). All pollen grains identified were Lithodora fruticosa (Boraginaceae) (Fig.
Diagrams of nest structures of nests of Hoplitis fertoni (right) and Osmia ferruginea (left). The nests are identified by locality snail codes (Cern – Cernuella sp., Ever – Eobania vermiculata, Iber – Iberellus sp., Olac – Otala lactea, Scan – Sphincterochila candidissima, Tpis – Theba pisana. Each box represents one brood cell, starting with the innermost cell on the left. Colours represent the various species recorded. White boxes represent intercalary cells.
We collected 58 shells with nests of O. ferruginea in nine of the 13 localities surveyed. Most nests (48) were collected in the localities of a dry hilly area. The remaining 10 nests were collected in the river floodplains. All nests were found exposed (not hidden) at ground level. The surface of the shells had no traces of masticated leaf matter. The closing plug was made of green masticated leaf matter (Fig.
Most nests (28, 48.3%) were built in Sphincterochila candidissima shells. The remaining nests were placed in shells of Eobania vermiculata (13, 22.4%), Cernuella sp. (11, 18.9%), Theba pisana (4, 6.9%), Iberellus sp. (1, 1.7%) and Otala lactea (1, 1.7%). The 58 nests collected contained 268 brood cells (mean ± SD: 4.6 ± 2.09; range: 1–9 brood cells per nest). The nests in S. candidissima shells contained 2–9 brood cells (mean 5.6, median 5), and those in E. vermiculata shells were similar 1–9 brood cells (mean 5.5, median 6). Nests in the smaller shells of Cernuella sp. and T. pisana contained fewer cells (range 1–5, mean 2.1, median 2 and range 2–3, mean 2.5, median 2–3, respectively).
Altogether 56 (20.9%) of the brood cells contained dead, dry or mouldy contents. Most of the remaining brood cells (203) contained pupae or adults of O. ferruginea, while 19 contained parasitoids (9% of brood cells containing alive insects). The main parasitoid species was Sapyga quinquepunctata (Sapygidae; 18 cells from 11 nests, all from locality S7; 19% parasitism). All the individuals of this cleptoparasitic species reached adulthood by late summer or beginning of autumn (September). Brood cells parasitized by S. quinquepunctata were recognizable by the dark brown oval-shaped cocoon, distinct from the cubic cocoons of O. ferruginea. The bombyliid Anthrax aethiops was recorded in a single cell of one nest. The structure of all nests is illustrated on Fig.
We analysed six pollen samples from nests collected at three different localities. Most pollen grains were of Cistaceae, Fabaceae (Cytisus type), and Lamiaceae (Table
Pollen composition of six provision samples from Osmia ferruginea nests.
Site | Pollen contents |
---|---|
S35 | Cistus albidus (Cistaceae) ca. 100%, Asteraceae and Thymus vulgaris (Lamiaceae) |
S37 | Cistus albidus (Cistaceae) 37 %, Cytisus scoparius (Fabaceae) 37 %, Olea europaea (Oleaceae) 26 % |
S37 | Cistus albidus (Cistaceae) 50%, Cytisus scoparius (Fabaceae) 40%, Olea europaea (Oleaceae) 10% |
S7 | Cistus albidus (Cistaceae) 48 %, Cytisus scoparius (Fabaceae) 27 %, Olea europaea (Oleaceae) 22 %, Thymus vulgaris (Lamiaceae)12 %, contamination of three pollen types of Asteraceae |
S7 | Thymus vulgaris (Lamiaceae) 51 %, Cytisus scoparius (Fabaceae) 49 % |
S7 | Cytisus scoparius (Fabaceae) 77 %, Thymus vulgaris (Lamiaceae) 23 % |
Nest structures of both species correspond to the nest descriptions published by previous authors (
The number of parasitic species associated with H. fertoni (5) in our study is remarkable. The most common parasitoid, Chrysura hybrida was already recorded on H. fertoni by
We also reared two species of velvet ants from the nests of H. fertoni. Velvet ants are ectoparasitoids and usually have a broad host spectrum. Some species preferentially parasitize either bees or wasps, but others have been recorded on both guilds of hymenopterans (
The bee-fly Anthrax aethiops, has been recorded as a parasitoid in nests of more than ten bee species, some of them nesting in gastropod shells (
Dioxys moesta is a cuckoo bee occurring in south Europe and North Africa. Its host spectrum is unknown. Other Dioxys species in Europe and neighbouring regions, are cleptoparasitic on bees of the family Megachilidae, mostly Hoplitis and Osmia (
Sapyga quinquepunctata is an unspecialized cleptoparasite in nests of several Megachilidae (
Analysis of the pollen provisions yielded contrasting results for the two species studied. Previous studies have reported Echium (Boraginaceae) as the only pollen source of H. fertoni (
The biology of shell-nesting bees from south Europe is poorly known. Our study contributes to filling this gap by providing new records of parasites and pollen use, as well life history and nesting behaviour traits. Interestingly, some of these traits are shared with bees of the same taxa nesting in other types of cavities. For example, Hoplitis adunca also lines cell walls, builds double inter-cell partitions and is oligolectic on Boraginaceae (
We would like to thank Guido Pagliano (Italy) for providing keys on Mutillidae, Lucy Boulton (UK) for the help with the English, and Georgina Alins and Neus Rodriguez-Gasol (IRTA, Lleida) for help with shell collection in the field. This study was supported by the Specific Research Project of University of Hradec Králové Nr. 2101/2019.