Full-Text Paper (PDF): Sex and breeding behaviour of the Sicilian snail-shell bee (Rhodanthidium siculum Spinola, 1838; ...
Arthropod-Plant Interactions DOI 10.1007/s11829-016-9489-x
ORIGINAL PAPER
Sex and breeding behaviour of the Sicilian snail-shell bee (Rhodanthidium siculum Spinola, 1838; Apoidea–Megachilidae): preliminary results Claudia Erbar1 • Peter Leins1
Received: 6 September 2016 / Accepted: 19 December 2016 Springer Science+Business Media Dordrecht 2017
Abstract In spring 2014 and 2016, we studied Rhodanthidium siculum in dunes south of Syracuse (Sicily). The females search for one of the frequently empty snail shells (mostly of Theba pisana), checking their size. In a suitable snail shell, a mixture of sand and saliva is deposited in the navel. A severe struggle among several males gets started. At every opportunity, the males try to copulate with the females. Large males occupy the snail shell that is used by the female to bring in pollen and nectar (preferably from Galactites tomentosus, Centaurea sphaerocephala, Glebionis coronaria and Lotus creticus). The procedure of harvesting lasts about 2–3 h, sometimes several hours. During this period, the female is visited for copulation every 2 min (initially even more frequently), preferentially by one large male, but small males occasionally mate as well. After laying one or two eggs, the female closes the snail shell with pieces of seashells or snail shells, aggregated with sand and saliva. The female transports the closed snail shell to a safe site. Depending on weather conditions, this may take several days. The maximum distance of movement observed was about 10 m. Finally, the completed snail shell will be buried, most often beneath a plant. The burial follows a certain pattern of movement.
Handling Editor: Isabel Alves dos Santos. In memoriam: Charles Duncan Michener (1918–2015) and Stefan Vogel (1925–2015) who influenced generations of entomologists and floral biologists all over the world. & Claudia Erbar
[email protected] 1
Centre for Organismal Studies Heidelberg, Biodiversity and Plant Systematics, Heidelberg University, Im Neuenheimer Feld 345, 69120 Heidelberg, Germany
Females ensure higher pollination efficiency than the males due to their higher flower constancy. Keywords Rhodanthidium siculum Multiple sex of bees Snail shell sealing Nest burying
Introduction The sexual and breeding behaviour of Rhodanthidium siculum (Spinola, 1838; the separation from the genus Anthidium was done by Isensee 1927) is almost unknown. In spring 2014 and 2016, we studied this bee species at two different sites about 40 km to the south of Syracuse (Sicily). The genus Rhodanthidium belongs to family Megachilidae/subfamily Megachilinae/tribe Anthidiini, characterized by the strong sternal (abdominal) scopa—the pollencarrying structure in the females—and lack of long hairs on the hind legs of females (Michener 2007). However, outside the Megachilidae, sternal scopae also occur, for example in the genus Ctenoplectra (Apidae), which mops up the oil from the flowers with an abdominal brush (Vogel 1981). Like other members of Anthidiini (Michener 2007), Rhodanthidium siculum differs from most other bee species because males are mostly significantly larger than females. The almost known fact on Rhodanthidium is that they use empty snail shells to build their nests (Peisl 1999). Many long-tongued bees (Apidae and Megachilidae) nest in a variety of existing holes, either naturally made or created by another organism. Some species, e.g. Osmia bicolor, even nest exclusively in empty snail shells (of Helicidae) as well (Michener 2007). Females of most bee species are monandrous, i.e. mate only once with a single male at the beginning of adult life
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(Michener 2007; Lampert et al. 2014). In Anthidiini, however, the females of the species studied so far are polyandrous and are receptive to males throughout their reproductive period (Alcock et al. 1977a; Eickwort and Ginsberg 1980; Paxton 2005). In Anthidiini, polyandry is combined with male territoriality and repeated copulations of the same individuals occur within a few minutes in both sexes (Severinghaus et al. 1981). In the case of Anthidium, the defended territories are the females’ food flowers. In general, when searching for females, male bees concentrate their activities in those locations where receptive females are most likely to occur. Males course over nest sites to mate with freshly emerged young females or patrol foodproviding flowers to pounce on females or seek females by congregating at specific assembly areas, so-called leks (Eickwort and Ginsberg 1980). Insect leks have been questioned (Eickwort and Ginsberg 1980), but we observed this behaviour in Chalicodoma sicula (family Megachilidae/subfamily Megachilinae//tribe Megachilini), a bee common at our Sicilian study sites. We present preliminary results of our project entitled ‘‘sex and breeding behaviour of the Sicilian snail-shell bee Rhodanthidium siculum’’, knowing well that our knowledge about this interesting hymenopter is still very limited. In this paper, we wish to demonstrate the high frequency of copulation (with different partners), the composition of larval supply in the snail shells used for breeding, and the sealing, transporting and burying of the filled snail shells.
(Asteraceae–Carduoideae), Galactites tomentosus, Glebionis coronaria, Lotus creticus L., Medicago marina L. (Fabaceae), Ononis natrix L. ssp. ramosissima (Desf.) Batt. (Fabaceae), Orobanche litorea Guss. (Orobanchaceae), Pistacia lentiscus L. (Anacardiaceae), Prasium majus L. (Lamiaceae), Pseudorlaya pumila (L.) Grande (Apiaceae), Silene colorata Poir. (Caryophyllaceae). Besides flower visits, we studied the sexual behaviour of the bees at the snail shells and in the surrounding area (e.g. on flowers) and the loading with the larval supply of 25 snail shells in detail (3 from Eobania vermiculata, 22 from Theba pisana) by fixed images and videos (Nikon COOLPIX P330, Nikon COOLPIX 7000). Six snail shells of different filling status were collected, stored at room temperature and later opened to investigate the pollen and nectar load; for the determination of nectar, we used glucose test strips (Medi-Test, Macherey and Nagel). In 2014, we collected (April 10, from site 1) one completely closed snail shell, kept it at room temperature under a bell jar and opened it in autumn (October 20) to study the larvae excrements. For the identification of the pollen grain load in the snail shells by SEM, we made a reference database of plants flowering in the vicinity of the occupied snail shells. Pollen grains were applied on a carbon conductive tab (mounted on an aluminium stub), coated with gold and studied in a Leitz (AMR 1200B) scanning electron microscope (software: Digital Image Processing System 2.6).
Results Materials and methods Morphology of the bee In 2014 we studied the sex and breeding behaviour of Rhodanthidium siculum at two sites (site 1 and 2) over two days and 2016 at one site (site 2) over nine days. Site 1 Sicily, Province of Syracuse, south of Noto, Riserva naturale orientata Oasi faunistica di Vendicari, about 200 m north of Tonnara di Vendicari; 10.?11.4.2014—the transition zone between a rocky plateau rising above a cliff and a ruderal site; main blooming plants at the rocky plateau: Chamaerops humilis L. (Arecaceae), Frankenia laevis L. (Frankeniaceae), Lotus creticus L. (Fabaceae), Moraea sisyrinchium (L.) Ker (Iridaceae), Limonium sinuatum (L.) Mill. (Plumbaginaceae); at the ruderal site: Ferula communis L. (Apiaceae), Glebionis coronaria (L.) Cass. ex Spach (Asteraceae–Asteroideae), Tragopogon porrifolius L. (Asteraceae–Cichorioideae). Site 2: Sicily, Province of Syracuse, south of Noto, dunes of a sandy cove north to the Zona Archeologica Eloro, covered with halophytes and salt tolerant plants typical of the area as well as more common plants; main blooming plants 12.4.2014?30.3.-8.4.2014: Centaurea sphaerocephala L.
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The relatively large bees are easily recognizable by their conspicuous brownish-yellow, clearly defined markings on the lateral abdomen. The males of Rhodanthidium siculum are, in general, significantly larger than the females. The males reach body lengths of 24–29 mm (two males measured), while the females measure 16–20 mm (four females measured). In addition, there are subordinate (i.e. non-territorial) males that are smaller than the territory-owning males but larger than the females. Apart from their different body size, males and females differ in their mandibles, as well as in the colour of their heads and mandibles. The mandibles are widest distally and three- to four-toothed. The lower tooth is larger in the male than in the slender female mandibles. Whereas the head, face and mandibles of the females are entirely black (Fig. 2a, e), the males have a yellow clypeus and the mandibles are yellow with a black border (Fig. 1c). The last tergit of the males is strongly trifid (broad, rounded median lobe with two lateral smaller projections).
Sex and breeding behaviour of the Sicilian snail-shell bee (Rhodanthidium siculum Spinola…
Fig. 1 Early phases of occupancy of an empty snail shell and main phase of copulation. a Deposition of sand–saliva mixture between aperture and navel of the shell (arrow; snail shell no. 6). b Frontal air fight of two rivalling males. c Large male ‘‘guarding’’ the snail shell in the absence and presence of the female (snail shell no. 5). d Large
male and female copulate near snail shell (snail shell no. 11). e Small male approaches while the female enters the snail shell onto which the large male is sitting. f Copulation of female with a small male while the large man (at the right) is ‘‘watching’’ (e, f: snail shell no. 3)
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Nest occupancy, copulation, nest provisioning After some exploratory flights, the female adopts one of the numerous empty snail shells. Most frequently, a shell of the Mediterranean coastal snail or sand hill snail, Theba pisana, is used as the brood site (the width of the used shells is 16–18 mm, the height 12–16 mm; 14 nests were measured with a calliper). Less frequently, shells of the chocolate-band snail, Eobania vermiculata (the width of the used shells is 21–23 mm, the height 14–18 mm; three nests measured), are used. The female repeatedly crawls deep into the snail shell. If the snail shell is suitable, the first action is to deposit sand between the aperture and the snail shell navel, the umbilicus (Fig. 1a). Often the female bee uses the sand which is mostly present inside the snail shell. These grains of sand are mixed with saliva. The mixture has a glass-like shine and becomes somewhat hardened (Fig. 1c, d). During the entire further work in the snail shell, the sand-saliva mixture is always found close to the umbilicus. Before the female undertakes her first foraging flights, she is incited by several males to copulate. Severe struggles among several males may take place. The males fight frontally in the air, aggressively attacking each other with open, sharp, pincer-like mandibles (Fig. 1b). As a rule, the larger of the two fighters is the winner and this large male then adopts the snail shell. The adopted snail shell and its immediate surroundings are the territory of this male for the time of nest provisioning by the female. When the female is on foraging flights or is inside the snail shell, the male may sit on the snail shell (Fig. 1c). When the male has left the snail shell for a short time and then comes back, he inspects the aperture of the snail shell. During this phase, when the female brings in pollen and nectar, the large male, the ‘‘owner of the snail shell’’, tries to copulate with the female as often as possible (Fig. 1d). The approaching female is intercepted and forced to copulate, mostly with high frequency. If he was not successful in catching the female during the approach, he drags the female out of the snail shell, whenever he can grasp the backside. This can be done using the legs or mandibles. Within short periods of time (10–20 s), copulation may take place repeatedly. Copulation takes place constantly with the female being seized by the male from behind (Fig. 1d). During the mating process, the head and thorax of the female are forward-turned and the male curves its abdomen into a sickle shape (up to a curvature of 180). The male tightly clasps the female with its legs to get himself into the correct position to insert his genital organ into the female genital tract (Fig. 1d), which can happen up to 10 times during one mating process (one can hear the clicking of the chitinous exoskeleton). At the end of the mating, the female tries to escape and both partners are
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often found in a sort of struggle when the female attempts to dislodge the male. The most common mating place is at or near the nesting site, the snail shell. However, occasionally, the males catch the females during a flower visit. Mostly, the pair then fells from the flower to the ground where copulation happens (Fig. 2d). When the large male copulates with ‘‘his’’ female or ‘‘guards’’ the snail shell with the female inside, often smaller (or, more infrequently, similar-sized) males approach the snail shell (Fig. 1e). Severe fighting takes place between the rival males in the air and on the ground. Fighting males, which fall to the ground, grapple for some time. As a rule, the large male is the winner and, immediately after the fight, he inspects the inside of ‘‘its’’ snail shell. Subsequently, mainly towards the end of the filling phase of the nest, small males more frequently attempt to copulate with the female. They are not always successful. However, the copulation even happens under the eyes of the ‘‘owner’’ of the snail shell (Fig. 1f). After the copulating pair has separated, the large male inspects the snail shell and, for his part, tries to copulate with ‘‘his’’ female. We observed (at least three records) that even two males, simultaneously, try to copulate with the female. Towards the end of the nest filling, the female repels the large (as well as small) male by attacking it with open mandibles (Fig. 2a). Nevertheless, during the entire process of filling the snail shell with larvae provisions (the procedure of harvesting lasts about 2–3 h, sometimes several hours) copulations occur, on average, every 3 min. The foraging flights of the females vary in length. As a rule (under the conditions of the 2016 observation period), the female’s absence from the nest lasts 7–9 min. In the cases of long absence, we could not ascertain the target flowers. However, in addition, short flights of the female are recorded. Short flights are undertaken to flowers in close vicinity to the nest. During a 2-min flight, for example, a female visited at least 10 flowers of Lotus creticus within a distance of 3–4 m from the nest. The filling process itself is difficult to observe since the female often places the snail shell with the aperture located horizontally (and not at the top); hence, the pollen-loaded underside of the female cannot easily be seen. However, a few observations indicate that during each foraging flight only the pollen grains of a single plant species are gathered in the scopa (Fig. 2b–d). A yolk-yellow colour of the collected pollen grains forming a sticky mass due to abundant pollenkitt (Fig. 2b, c) allows assigning these pollen grains to Glebionis coronata. Whitish pollen load (Fig. 2d) cannot be unequivocally assigned to a certain species since several flowers of the surrounding area have
Sex and breeding behaviour of the Sicilian snail-shell bee (Rhodanthidium siculum Spinola…
Fig. 2 Provisioning of the nest and snail shell closure by the female. a Arriving female attacks the male with open mandibles. b, c One filling event; arrows indicate the yolk-yellow pollen load (Glebionis coronata) in the sternal scopa (a–c snail shell no. 20). d Whitish pollen load (arrow) in the scopa. e Female leaving the snail shell head
first while the large male is ‘‘guarding’’ the snail shell (snail shell no. 5). f, g Different phases of snail shell closure; arrow in (f) indicates inner ring of sand mixed with saliva, arrow in (h) indicates thread of slime (f snail shell no. 6, g no. 2, h no. 11, i no. 1)
cream-white pollen grains (Centaurea sphaerocephala, Galactites tomentosus, Lotus creticus). However, concerning the scopa shown in Fig. 2d, it is most likely pollen from Lotus creticus, because we observed just before this
that the male pounced on the female while it was exploring a Lotus flower. After a foraging flight, the female seems at first to regurgitate nectar and then the pollen grains are wiped
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from the scopa. In doing so, the female should turn around. However, we could only twice take a photo showing that the female leaves the snail shell head first (Fig. 2e) and not backwards, as is usual. During the filling period, mostly the females rotate the snail shell more or less on the spot. But some females did not do this. Closure of the snail shells After several loadings with nectar and pollen, the closure of the still sparsely filled snail shell is initiated. For this purpose, the female forms a ring of sand on the inner side of the snail shell near the opening, using the sand lying between the opening and the snail shell’s navel (Fig. 2f). In doing so, sand seems to be mixed with saliva. The ring of sand has a glass-like shine. Threads of slime are often visible between the agglutinated sand and the mouth opening of the female. When the provision is completed and one or two eggs have been laid, the snail shell will be completely closed (Fig. 2g–i). During the early sealing phase, ‘‘sexual harassment at work’’ occurs, although with decreasing frequency (on average every 5 min). The larvae will later develop on the provision, the mixture of pollen and nectar. In one of the artificially opened snail shells that were closed on the same day (2016), we found one egg (Fig. 3h). In the snail shell opened in October 2014, two young female bees were found. We did not observe any partition in the snail shell between the two females. The final closure of the snail shell by the female may take several hours. The female uses mainly the mandibles and the head, but the forelegs as well. If the procedure is interrupted by bad weather conditions, it will be continued the following day. The completed sealing cover is comparable to a terrazzo floor. Larger and smaller fragments of snail shells and seashells are arranged and then grouted with sand and saliva (Fig. 2i). At first, suitable pieces are placed on the inner sand ring (Fig. 2f). Sometimes a quite cumbersome handling with large, non-fitting pieces can be observed (Fig. 2g). Finally, however, fitting pieces are brought or non-fitting pieces are cut with the strong mandibles. Again and again, saliva is used as glue. At first, it is stringy (Fig. 2h); later, it hardens into a glass-like form. At the end of the closing procedure, the shell-terrazzo floor is often covered with a sand layer. Transportation and burying of the nests The last action, which may last hours or days (depending on the position of the snail shell and weather conditions), is the burying of the completely sealed snail shell. The object
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is to transport the snail shell to an appropriate site, i.e. welldrained, loose and aerated soil, mostly in the root area of perennials such as the bulbous sea daffodil (Pancratium maritimum, Amaryllidaceae) and the suffruticose Cretan bird’s foot trefoil (Lotus creticus, Fabaceae). The hard transport happens centimetre for centimetre, uphill and downhill in the wavy sand surface. The transport is achieved using the hind legs, whereby the insect rests the front of its head on the sand (Fig. 3a, b). The largest distance that we can record amounts to about 10 m. Upon arriving at a suitable site, the female deposits the snail shell in such a way that the sealed opening is directed to the bottom and laterally to the hole that will be excavated (Fig. 3c). Then the female climbs, at first forwards, over the snail shell (Fig. 3d), grasps with its mandibles (and only with the mandibles!) a lump of sand, then runs again over the snail shell, now backwards, and deposits the lump of sand some distance (a few cm) from the snail shell. During the depositing process, the forelegs are used as well. After countless runs over the snail shell, a hole has arisen (Fig. 3e) into which the snail shell is pushed by the bee (Fig. 3f). Finally, the cavity is filled with sand. The maximum depth we measured was 2 cm (from the top of the snail shell). However, the snail shells may lie close to the soil surface, i.e. when roots are close to the cavity. During the phases of transport and burying, no harassing male could be observed any more. Flower visits Male individuals of Rhodanthidium siculum visit flowers only for their own energy demands. The variety and the frequency of the visited flowers are relatively high. Frequently we found males searching for nectar on flowers of Centaurea sphaerocephala, Galactites tomentosus and Lotus creticus, and less frequently on Borago officinalis, Lathyrus clymenum, Medicago marina, Orobanche litorea and Prasium majus (Table 1). We observed that males switched between flowers of Borago, Lathyrus and Medicago. Another male changed repeatedly between Orobanche and Lotus. Other males visited successively different flower heads of Centaurea. Females were found visiting the flowers of Centaurea sphaerocephala, Galactites tomentosus and Lotus creticus (Table 1), where they collect nectar as well as pollen grains. In one case, the load in the scopa (which could rarely be observed) could be determined as pollen of Glebionis coronata (Asteraceae), judged from the pollen colour and abundant pollenkitt (Fig. 2b, c). However, we never observed female Rhodanthidium siculum individuals as visitors on the inflorescences of Glebionis, although there are large populations in the study areas.
Sex and breeding behaviour of the Sicilian snail-shell bee (Rhodanthidium siculum Spinola…
Fig. 3 a–f Transportation and burying of a sealed snail shell by the female. a, b Transport (snail shell no. 12). c–f Image sequence of snail-house burying (snail shell no. 13) in the root area of Pancratium maritimum. g–h Larvae provision. g Closed snail shell (no. 2)
partially opened to show the pollen/nectar provision mass. h Snail shell (no. 6) cut open after the egg (E) has been laid; arrow indicates the inner ring of sand mixed with saliva
Pollen grains in the larvae provision and excrements
Small quantities are found from pollen of Tragopogon porrifolius, Silene colorata and Acanthus spinosus, as well as from a few unidentified pollen grains (Table 1). Mostly the pollen grains of the different species are mixed up (perhaps due to the turning of the snail shell in different positions; Fig. 4a–b), but sectors in which one species dominates may also be found. Pollen grains in the faecal pellets (in a snail shell collected from site 1) have an intact exine structure, i.e. they are not damaged by the larvae mouthparts. The faecal pellets investigated mainly contain a mixture of Glebionis coronaria and Galactites tomentosus, and more pollen grains of Tragopogon porrifolius than in the provision of site 2, corresponding to the more ruderal site 1.
The pollen/nectar provision mass mostly has a dark yellow colour (Fig. 3g). The mass may look homogeneous or crumbly and sticky sections may occur side by side. The latter can mainly be observed in snail shells that are not yet closed. But the analysis of the different sections has shown that there is no significant difference in the distribution of pollen grains. The content of nectar may vary, but, as a rule, the pollen grains are embedded in nectar (Fig. 3g). The following pollen grains are present in larger amounts in the provisions inside the snail shells (from site 2): Galactites tomentosus, Glebionis coronaria, Centaurea sphaerocephala and Lotus creticus (Fig. 4a–b; Table 1).
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C. Erbar, P. Leins Table 1 Flower visits of males and females and occurrence of pollen grains in the brood provisions; three categories of frequency (estimated): xxx = frequent, xx = occasional, x = rare Species
Recorded visits #
Pollen in larvae provisions (site 2) $
Acanthus spinosus (Acanthaceae)
x
Borago officinalis (Boraginaceae)
x
Centaurea sphaerocephala (Asteraceae–Carduoideae) Galactites tomentosus (Asteraceae–Carduoideae)
xxx xxx
xxx xxx
Glebionis coronaria (Asteraceae–Asteroideae) Lathyrus clymenum (Fabaceae)
xxx xxx xxx
x
Lotus creticus (Fabaceae)
xxx
Medicago marina (Fabaceae)
x
Orobanche litorea (Orobanchaceae)
xx
Prasium majus (Lamiaceae)
x
Silene colorata (Caryophyllaceae)
xxx
xxx
x
Tragopogon porrifolius (Asteraceae–Cichorioideae)
xx
Pollen indet.
x
Fig. 4 Pollen grains in the larvae provision (from snail shell no. 9; after solution of the pollen/nectar mass in water). C–Centaurea sphaerocephala (Asteraceae–Carduoideae); Ga–Galactites tomentosus
(A.–Carduoideae); Gl–Glebionis coronaria (A.–Asteroideae); L–Lotus creticus (Fabaceae)
Discussion
pebbles and mud) and leaf pieces, further plant material such as plant hairs and resin. The materials may be combined in various ways (e.g. Michener 2007). Osmia bicolor, the two-coloured mason bee, is perhaps the best known of the snail shell-nesting Osmia species. It uses chewed leaf material for building and sealing the cells, and covers the completed snail shell with a pile of pine needles or dry grass blades (Westrich 1989). The chewed up leaf material forms (due to the saliva) a kind of ‘‘plant cement’’, which is, together with small pebbles and wood particles, used for the plug sealing the snail shell. Other snail shell-nesting Osmia species use small fragments of broken shells that are cemented with the leaf pulp (e.g. O.
Nest construction Megachilid genera are most commonly known as mason bees (e.g. Chalicodoma parietina, C. sicula, Hoplitis anthocopoides) and leafcutter bees (e.g. Megachile rotundata). The names describe the materials—soil or leaves— they use to build their nest cells. Others collect plant hairs for this purpose and are called wool-carder bees (e.g. Anthidium manicatum). The materials used for building the nests are diverse and include, apart from different soil particles (such as sand,
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Sex and breeding behaviour of the Sicilian snail-shell bee (Rhodanthidium siculum Spinola…
melanura, Mu¨ller 1992, 2016; O. rutila, Haeseler 1997). The resin bees (e.g. Anthidium [Anthidiellum] strigatum) construct isolated, single cells made of resin (Bellmann 1977, 1981, 2010; Westrich 1989). Among the snail shell-nesting Rhodanthidium species, the use of resin in nest construction and sealing is reported in R. sticticum and R. septemdentatum (Ferton 1908; Pasteels 1977). Gotlieb et al. (2014) label R. siculum as ‘‘resin bee’’, given that fragments of a nest of R. siculum quickly melted when placed on a heating plate, burned when passed through a flame, and did not dissolve in water. However, we never observed the transport of resin into the snail shell and, additionally, found that all parts of the nest filling can be easily dissolved in water, which contradicts the assumption of resins being present in the nest. Since our studies do not confirm the use of resin in nest construction and sealing, we propose the vernacular name ‘‘Sicilian snail-shell bee’’. For grouting the pieces of snail shells and seashells, sand mixed with saliva is used as cement. Notable are the glass-like shine and the viscous threads visible between the agglutinated sand and the mouth opening of the female (Fig. 2h). A labial gland secretion is involved in the hard clay nests of Chalicodoma sicula (family Megachilidae/subfamily Megachilinae//tribe Megachilini). The nests adhering to branches and twigs of bushes, stones or buildings are made of a mixture of sand and a labial secretion (composed of long-chain hydrocarbons). They are hydrophobic and are not destroyed by rain for several years (Kronenberg and Hefetz 1984). The chemical nature of the viscous threads becoming glass-like in Rhodanthidium siculum has to be investigated. Nesting in snail shells: a comparison In Megachilidae, nests may be free standing constructs situated on rocks, walls, stems or twigs; they may also be in the soil, in holes in wood or plant stems, or in diverse cavities (e.g. Michener 2007). Some species are known to use empty snail shells for nest construction. Among the Osmia species nesting in snail shells, O. melanura, O. sybarita, O. rutila and O. rufigastra are known to transport their nests when they have been completed and to bury them (Mu¨ller 1992; Haeseler 1997). When O. rutila has closed the snail shell, it moves the snail shell over distances more than 3 m to a place in the vicinity of plants. Then the bee digs a slanting hole, rolls the snail shell to the hole, pulls it in the hole and finally scraps sand on the snail shell (Haeseler 1997). We observed that Rhodanthidium siculum transports the closed snail shell up to 10 m away from the site of nest filling. The behaviour of R. siculum when burying the snail shell deviates from O. rutila in that the bee crawls over the snail shell again and again, grasps with its mandibles a lump of
sand and deposits the lump of sand some distance from the snail shell. After countless runs over the snail shell, the bee pushes the snail shell deeper into the created hole and fills up the hole with sand. The result is the same: The snail shell lies in a certain depth in the sand soil. Thereby, the specialists that are dependent on costal dunes and snail shells minimize the unpredictable risks of the environment (blowing away by storms, damage by predators, high temperatures on the soil surface). In R. siculum, sometimes more time is spent in this optimized protection of one to two eggs in the snail shell than in the time invested in cell provisioning. Depending on the surrounding and weather conditions, the transportation and burying of the closed snail shell may last several days. How do the females recover their nest? Scent seems to play a crucial role. We conducted small experiments: To test the retrieval of snail shells in the phases of filling, transportation and burying, we dislocated snail shells by a few centimetres to 1 m. The females easily found their snail shell. Scent seems also to be important in attracting the male. In the early phase of nest occupying, the deposition of the sand–saliva mixture obviously serves to attract males and is the signal to the males for copulation. Perhaps the saliva contains attractants. When the male has left the adopted snail shell for a short time and comes back, he inspects the aperture of the snail shell, perhaps attracted by the female’s scent or leaving a scent mark itself. Flower visits and nest provision Megachilidae are solitary bees whose pollen-carrying structure, the so-called scopa, is restricted to the ventral surface of the abdomen, rather than mostly or exclusively on the hind legs as in other bee families (Michener 2007). The plant families Asteraceae and Fabaceae–Faboideae are particularly suited to the bees with abdominal brushes as, with few exceptions, they present their pollen from below and the bees can scrape it directly into the brush (Proctor et al. 1996). A broad analysis has shown that by far the most important pollen source of the anthidiine bees as a whole are Asteraceae (41.7%; tribe Cardueae: 28.0%), followed by Fabaceae– Faboideae (23.1%) and Lamiaceae (13.0%; Mu¨ller 1996). In the abdominal scopae of R. siculum, Asteraceae as a whole contribute 56.8% (and its tribe Cardueae 46.3%) to the pollen spectrum and the Fabaceae–Faboideae 14.5% (30 pollen loads were analysed in the scopae from 26 different localities, obtained from museum, university and private collections; Mu¨ller 1996). Although we did not do a detailed quantitative study, we can confirm the prevalence of Cardueae pollen grains (Centaurea sphaerocephala, Galactites tomentosus). In smaller amounts pollen grains of Lotus creticus (Fabaceae–Faboideae) and Glebionis coronaria
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(Asteraceae–Asteroideae) are found in the larvae provision. All the frequently visited flowers provide both pollen and nectar and exhibit pump mechanisms of secondary pollen presentation (Leins and Erbar 2010). Glebionis has the pump mechanism common in Asteraceae–Asteroideae and Centaurea and Galactites exhibit the modified pump mechanism of Carduoideae–Cardueae. In both mechanisms, pollen grains are presented above the anther tube (Leins and Erbar 2010) and can easily be collected with the abdominal scopa. In the special pump mechanism of Lotus, called the ‘‘noodle squeezer’’ mechanism (=‘‘Nudelspritzenmechanismus’’), pollen is released onto the abdomen of the bee through a small hole at the tip of the keel when the keel is pressed down (Leins and Erbar 2010). Females ensure higher pollination efficiency than the males due to their higher flower constancy. The males visit a higher spectrum of flowers (Table 1). However, since males visit several flowers during one supply flight, they may be efficient pollinators, too. Competing flower visitors on the flowers of Glebionis and Galactites are various butterflies (also visiting Centaurea sphaerocephala) and the mining bee Dasypoda hirtipes (Melittidae/Dasypodainae), which has an enormous pollen-carrying capacity in the pollen brushes of its hind legs. A strong competitor for the Lotus flowers is the Sicilian mason bee Chalicodoma sicula (Megachilidae/ Megachilinae). At our study sites, Lotus creticus was the only pollen and nectar source for their larvae supply (at another site, nectar and pollen from another Fabaceae, namely Hedysarum glomeratum, was equally collected; personal observation). Chalicodoma can be described as oligolectic as can some more megachilid species (Mu¨ller 1996; Mu¨ller and Bansac 2004), collecting pollen exclusively from related plant species or genera. A bee is called polylectic if it collects pollen from flowers of a variety of unrelated plants. Thus, Mu¨ller (1996) classified Rhodanthidium siculum as polylectic. However, to bridge the gap between extremes, new categories such as eclectic oligolecty (95% or more of the pollen grains counted belong to the same two to four plant genera from two or three plant families) and mesolecty (95% or more of the pollen grains counted belong to two or three plant families and the most important group contributes less than 70%) were introduced (Cane and Sipes 2006; Mu¨ller and Kuhlmann 2008). Since we did not count the pollen grains in the scopae, we cannot decide whether R. siculum is eclectically oligolectic or mesolectic. Bees such as Megachilidae that have ventral scopae in which pollen is densely packed may still have much pollen available for transfer to stigmas (Thorp 2000). However, it must also be remembered that the amount of pollen lost from flowers for bee nutrition is surprisingly high.
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Depending on both bee species and host plant, up to 95.5% of the pollen produced by a flower can be collected by bees for their offspring (Schlindwein et al. 2005; Mu¨ller et al. 2006). Nevertheless, sufficient pollen grains reach the stigmas: The number of pollen grains deposited on the stigma is mostly several times higher than the number of ovules (Erbar and Enghofer 2001; Schlindwein et al. 2005). Based on the given data, one can calculate a P/S–O value, which relates the total number of pollen grains (P) that are deposited onto the stigmata (S) at the end of female anthesis to the number of ovules (O). This value not only provides information on the dimension of pollen tube competition (as the basis of a prezygotic selection), but also is an indicator for pollination efficiency. The reliability of the pollinators increases efficiency. Under these premises, we can conclude that due to the high frequencies of flower visits and the limited number of plant species foraged for pollen and nectar, the females of Rhodanthidium siculum are efficient pollinators. Multiple matings Since each mating offers an opportunity to father offspring, males can generally increase their fitness by mating with many females and high mating rates are typically associated with high male reproductive success (Arnquist and Nilsson 2000). Males produce sperm, small gametes, and females produce eggs, larger gametes. With the same investment of metabolic resources, an individual can produce a much larger number of sperms than eggs. This generates the simple prediction that a male will attempt to achieve as many fertilizations as possible, thereby maximizing his genetic success (Alcock 1980). In most species of Anthidiini, males are mostly significantly larger than females (Michener 2007) and vary greatly in size (Severinghaus et al. 1981). In many Anthidium species, the relative size is important since large males consistently outcompete smaller males in the fight for territories, namely the foraging sites of the females, and thus, their reproductive success is higher (e.g. Severinghaus et al. 1981; Villalobos and Shelly 1991; Starks and Reeve 1999, Payne et al. 2010). In the case of Rhodanthidium siculum, the males do not defend a foraging site against other males but another area essential to the females, namely the nesting site, the snail shell that was chosen by the female for nesting. Intrasexual competition of males for territories has probably selected for large body size of males (Wirtz et al. 1992). Nevertheless, although most matings are performed by territory owners, subordinate males do occasionally copulate (Alcock et al. 1977a). Our studies confirm this for Rhodanthidium siculum. The males are polygynous: Large males repeatedly mate with the same female. However, the
Sex and breeding behaviour of the Sicilian snail-shell bee (Rhodanthidium siculum Spinola…
male leaves the territory, the nesting site, when the female is in the closure phase of the snail shell and then adopts a new empty snail shell selected by another female. The small males have an alternative strategy. Because they mostly cannot win the struggle for the nest, they pursue a ‘‘sneaking strategy’’ (cf. Severinghaus et al. 1981 and Lampert et al. 2014 for Anthidium manicatum). Whenever possible, they copulate with a female either when the large male is absent from the nest during a foraging flight or if he tolerates the mating (after several matings perhaps he is exhausted; Fig. 1f). In addition, small males pounce on females while these are exploring flowers or sealing a snail shell. Most female bees collect enough sperm after a single copulation and store it in the spermatheca (receptaculum seminis); hence, monandry could be expected. Since males try to mate further, females may expend time and energy trying to repel and avoid males in such monandrous systems. In addition, taking part in multiple matings takes time away from foraging for brood provisions (Alcock et al. 1977a; Alcock 1980). The females of Rhodanthidium siculum are polyandrous because they mate during the nest construction repeatedly with large and small males, and may start after the burying of the completed nest with the preparation of another snail shell, accompanied by subsequent matings. It has been clearly demonstrated in Anthidium manicatum that males that copulate late in a sequence of mating partners have an above-average chance of siring the about-to-be laid egg of a female (Lampert et al. 2014). Obviously, sperm from sequential mates do not mix within the female. We do not know whether only the last mating male is likely to fertilize the egg in Rhodanthidium siculum. If we conversely assume that sperm of sequential matings is somewhat mixed in Rhodanthidium siculum, this would result in an advantage for the population. Perhaps, there is a genetic disposition of the different body sizes of the females, which would be advantageous for the breeding success in correlation with the different snail-shell sizes. A much greater variety of snail shells can be used by females of different sizes than the females were of the same size. The precondition would be that the different body size of the males is genetically fixed by the egg cell of a female and can be transferred to the females of the next generation by fertilization of an egg cell (the males are haploid). A further precondition would be that small males are successful in fertilization, too. However, factors such as the abundance of food resources and maternal age may be responsible for both large and small male offspring, too (Alcock et al. 1977b). Acknowledgements We are very grateful to Dr. Vollrath Wiese (Natural History Museum, Cismar, Germany) for confirming our determination of the snails.
References Alcock J (1980) Natural selection and the mating systems of solitary bees. Am Sci 68:146–153 Alcock J, Eickwort GC, Eickwort KR (1977a) The reproductive behavior of Anthidium maculosum (Hymenoptera: Megachilidae) and the evolutionary significance of multiple copulations by females. Behav Ecol Sociobiol 2:385–396 Alcock J, Jones CE, Buchmann SL (1977b) Male mating strategies in the bee Centris pallida Fox (Anthophoridae: Hymenoptera). Am Nat 111:145–155 Arnquist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145–164 Bellmann H (1977) Beobachtungen zum Brutveralten der Harzbiene Anthidiellum strigatum (Hymenoptera: Megachilidae). Ent Germ 3:356–361 Bellmann H (1981) Zur Ethologie mitteleuropa¨ischer Bauchsammlerbienen (Hymenoptera, Megachilidae): Osmia bicolor, O. rufohirta, Anthidium punctatum, Anthidiellum strigatum, Trachusa byssina. Vero¨ff. Naturschutz Landschaftspflege Bad.Wu¨rtt. 53(54):477–540 Bellmann H (2010) Bienen, Wespen, Ameisen: Hautflu¨gler Mitteleuropas, 3rd edn. Franckh-Kosmos Verlag, Stuttgart Cane JH, Sipes S (2006) Characterizing floral specialization by bees: analytical methods and a revised lexicon for oligolecty. In: Waser NM, Ollerton J (eds) Plant-pollinator interactions: from specialization to generalization. University of Chicago Press, Chicago, pp 99–122 Eickwort GC, Ginsberg HS (1980) Foraging and mating behavior in Apoidea. Ann Rev 25:421–446 Erbar C, Enghofer J (2001) Untersuchungen zum Reproduktionssystem der Wegwarte (Cichorium intybus, Asteraceae): Pollenportionierung, Narbenbelegung und Pollenschlauchkonkurrenz. Bot Jahrb Syst 123:179–208 Ferton C (1908) Notes de´tache´es sur l’instinct des hyme´nopte`res mellife`res et ravisseurs (4e`me se´rie) avec la description de quelques espe`ces. Ann Soc Entomol Fr 77:535–586 Gotlieb A, Pisanty G, Rozen JG, Mu¨ller A, Ro¨der G, Sedivy C, Praz C (2014) Nests, floral preferences, and immatures of the bee Haetosmia vechti (Hymenoptera: Megachilidae: Osmiini). Am Mus Novit 3808:1–20 Haeseler V (1997) Osmia rutila, a wild bee occurring in the coastal area of the southwest Mediterranean where it is now in danger of extinction. In: Garcia Nova F, Crawford RMM, Diaz Barradas MC (eds) The ecology and conservation of European dunes. Sciencias, Univ, Sevilla, pp 169–183 Isensee R (1927) A study of the male genitalia of certain anthidiine bees. Ann Carnegie Mus 17:371–382 Kronenberg S, Hefetz A (1984) Role of labial glands in nesting behaviour of Chalicodoma sicula (Hymenoptera; Megachilidae). Physiol Entomol 9:175–179 Lampert KP, Pasternak V, Brand P, Tollrian R, Leese F, Eltz T (2014) ‘Late’ male sperm precedence in polyandrous wool-carder bees and the evolution of male resource defence in Hymenoptera. Anim Behav 90:211–217 Leins P, Erbar C (2010) Flower and fruit. Morphology, ontogeny, phylogeny, function and ecology. Schweizerbart Science Publishers, Stuttgart Michener CD (2007) The bees of the world. Johns Hopkins University Press, Baltimore Mu¨ller A (1992) Osmia melanura Morawitz, 1871, eine helicophile Bienenart aus dem Mittelmeerraum (Hymenoptera, Megachilidae). Entomofauna 13:273–280
123
C. Erbar, P. Leins Mu¨ller A (1996) Host-plant specialization in western palearctic anthidiine bees (Hymenoptera: Apoidea: Megachilidae). Ecol Monogr 66:235–257 Mu¨ller A (2016) Palaearctic Osmiine Bees. ETH Zu¨rich. http://blogs. ethz.ch/osmiini. Accessed 1 Sept 2016 Mu¨ller A, Bansac N (2004) A specialized pollen-harvesting device in western Palaearctic bees of the genus Megachile (Hymenoptera, Apoidea, Megachilidae). Apidologie 35:329–337 Mu¨ller A, Kuhlmann M (2008) Pollen hosts of western palaearctic bees of the genus Colletes (Hymenoptera: Colletidae): the Asteraceae paradox. Biol J Linn Soc 95:719–733 Mu¨ller 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. Biol Conserv 130:604–615 Pasteels JJ (1977) Une revue comparative de l’e´thologie des Anthidiinae nidificateurs de l’ancien monde. Ann Soc Entomol Fr 13:651–667 Paxton RJ (2005) Male mating behaviour and mating systems of bees: an overview. Apidologie 36:145–156 Payne A, Schildroth DA, Starks PT (2010) Nest site selection in the European wool-carder bee, Anthidium manicatum, with methods for an emerging model species. Apidologie 42:181–191. doi:10. 1051/apido/2010050 Peisl P (1999) Beobachtungen und Gedanken zum Verhalten von Bienen-Ma¨nnchen. Bembix 12:21–25
123
Proctor M, Yeo P, Lack A (1996) The natural history of pollination. Timber Press, Portland Schlindwein C, Wittmann D, Martins CF, Hamm A, Siqueira JA, Schiffler D, Machado IC (2005) Pollination of Campanula rapunculus L. (Campanulaceae): How much pollen flows into pollination and into reproduction of oligolectic pollinators? Plant Syst Evol 250:147–156 Severinghaus LL, Kurtak BH, Eickwort GC (1981) The reproductive behavior of Anthidium manicatum (Hymenoptera, Megachilidae) and the significance of size for territorial males. Behav Ecol Sociobiol 9:51–58 Starks PT, Reeve HK (1999) Condition-based alternative reproductive tactics in the wool-carder bee, Anthidium manicatum. Ethol Ecol Evol 11:71–75 Thorp RW (2000) The collection of pollen by bees. Plant Syst Evol 222:211–223 Villalobos EM, Shelly TE (1991) Correlates of male mating success in two (Hymenoptera: Megachilidae) species of Anthidium bees. Behav Ecol Sociobiol 29:47–53 Vogel S (1981) Abdominal oil-mopping—a new type of foraging in bees. Naturwissenschaften 68:627–628. doi:10.1007/BF00398624 Westrich P (1989) Die Wildbienen Baden-Wu¨rttembergs. 2 Bde. Ulmer, Stuttgart Wirtz P, Kopka S, Schmoll G (1992) Phenology of two territorial solitary bees, Anthidium manicatum and A. florentinum (Hymenoptera, Megachilidae). J Zool 228:641–651