IDENTIFICATION OF PLANT SPECIES VISITED BY RHODANTHIDIUM STICTICUM

Our field surveys showed a high diversity of plants on which R. sticticum feeds (Appendix 1). In particular, 43 species and 13 families of flowering plants from NE, C and SE of the Iberian Peninsula were identified. Among them, Papilionaceae (8 spp.), Lamiaceae (12 spp.) and Plantaginaceae (5 spp., all of them Antirrhineae) were the most frequently visited (Appendix 1). From literature, 38 more species belonging to 14 families were retrieved (Appendix 2). Therefore, polylecty appears to be predominant in Rhodanthidium sticticum diet. Despite that, R sticticum shows a clear attraction for Antirrhinum species.

FLIGHT ABILITY, TERRITORIALITY AND MATING

Males spend most of the time patrolling their territories (estimated 75% of the time), looking for females (Fig. 3) or resting on nearby rocks and branches, usually promontories where they can warm up on the sun while they watch their area. From time to time, they visit the flowers in their territory to feed on nectar, but they do this activity more rarely. Rhodanthidium sticticum males also perform exploratory flights when a new object enters their territory (a bag or a camera, for example), during which they remain in static flight in front of the object, observing it directly. Females spend their time looking for suitable shells for nesting, building the nest, feeding on nectar and collecting pollen for their offspring (Fig. 4).

Fig. 3.— Male of Rhodanthidium sticticum watching a female feeding on Antirrhinum microphyllum. Fig. 3.— Macho de Rhodanthidium sticticum vigilando a una hembra mientras esta visita una flor de Antirrhinum microphyllum.

Fig. 4.— a. Female of Rhodanthidium sticticum visiting flowers of Antirrhinum microphyllum. b. Close-up of a female of R. sticticum visiting flowers of A. microphyllum. Fig. 4.— a. Hembra de Rhodanthidium sticticum visitando flores de Antirrhinum microphyllum. b. Primer plano de una hembra de R. sticticum visitando flores de A. microphyllum.

Males protect territories with abundant flower patches, showing preference for Antirrhinum, Labiatae and Papilionaceae shrubs. They show a ferocious defence of the territory, chasing, attacking and striking other male intruders, but also other bees of similar or bigger size (including much bigger bumblebees or Xylocopa violacea (Linnaeus, 1758) individuals) and other flying insects that happen to enter their surveillance area, like flies or butterflies. We did not observe Rhodanthidium males attacking small flying insects in their territories.

A number of mating attempts end up in failure. Females are reluctant to the copula, so males try to catch them unaware. When a female detects the proximity of a male while feeding or collecting nectar, quickly take flight to avoid it (Fig. 5). Contact between a male and a female does not guarantee mating, either. Frequently, females wriggle out before males are able to copulate. If other male candidates are around, they usually interrupt the copula by trying to force the first male out and get the female. Even if the male has been able to start intercourse with the female, sometimes they become too heavy for the stems they are leaning on and they fall, allowing the female to escape (Fig. 6). During a successful intercourse (Fig. 7), a very characteristic sound, a continuous, rhythmic, dry clickety-clack noise can be heard, caused by the hitting of the cuticles.

Fig. 5.— Female of Rhodanthidium sticticum facing a male who was trying to copulate. Fig. 5.— Hembra de Rhodanthidium sticticum enfrentándose a un macho que intenta copular con ella.

Fig. 6.— a. Male of Rhodanthidium sticticum unsuccessfully trying to mate while a female was visiting flowers of Antirrhinum microphyllum. b. Male of R. sticticum harassing a female and unsuccessfully trying to copulate with it while it fed on flowers of A. microphyllum. Fig. 6.— a. Macho de Rhodanthidium sticticum intentando, sin éxito, copular con una hembra mientras esta visita flores de Antirrhinum microphyllum. b. Macho de R. sticticum acosando a una hembra e intentando, sin éxito, copular con ella mientras se alimenta en flores de A. microphyllum.

Fig. 7.— Rhodanthidium sticticum copulating. Fig. 7.— Rhodanthidium sticticum copulando.

PHENOLOGY

Rhodanthidium sticticum is a very active bee during the flowering period of most Spring flowers, from March until June, but in warmer areas it is usual to find it as early as February. Most of records were taken between March and May, enlarging until mid June, matching the data from other areas of the species (Morocco, Algeria and Sicily: Kasparek & Lhomme, 2019; Algeria: Aguib et al., 2010). There are no records in literature or in collections about the presence of the species later than June, despite Kasparek (2019) stating, without providing any evidence (“an early spring and late autumn species with possibly two generations per year”) and that it was found in Spain in October/November. It seems to be, however, an univoltine species, like R. siculum or other Anthidiini bees (Anthidium florentinum, Fortunato et al., 2013). Flying period for this species starts early and is relatively long, similar to R. septemdentatum (Kasparek, 2019) but longer than R. siculum (Ortiz, 1990; Aguib et al. 2010; Erbar & Leins, 2017), probably due to the fact that R. siculum is associated to warmer climate and its optimal period is shorter (Romero et al., 2020a).

SHELTERING IN SHELLS

Our results show that R. sticticum is active in sunny, not windy days, as most of the records on the flight were obtained under those conditions, corroborating previous observations by other studies (Torres et al., 2001; Romero et al., 2020a). However during cloudy, rainy and windy days, or at the late afternoon, R. sticticum bees were mostly found sheltering inside snail shells. Apparently, Afranthidium hamaticauda Pasteels, 1984, A. odonturum (Cockerell, 1932) (Gess & Gess, 1999, 2008, 2014) and Hoplitis conchophila Kuhlmann, 2011 (Kuhlmann et al., 2011) also use snail shells for sheltering, but this behaviour has rarely been described. In those cases, the authors did not provide any information about the weather conditions or the time of the day they did their records at, but considering the location (the Namibian desert) the use for sheltering is, most likely, against the heat of the central hours of the day or to sleep at night. Despite the existence of detailed descriptions of the nesting behaviour of Rhodanthidium bees inside snail shells (Pasteels, 1977; Erbar & Leins, 2017), sheltering has never been described before on this species.

Of all the bees found in shells, 30% were sharing and most of them were males. This behaviour is in contrast with the territoriality usually showed when they are flying and there are no previous records of other bees in their adult phase sharing shells. The reasons could be diverse. Individuals sharing the same shells they were born from (phylopatry), high density of individuals and few shells disposable, which would force them to share, or the urge to rapidly find a shelter when the weather suddenly changes. The fact that most of the sharing bees were males is probably due to the higher proportion of males. The male-female proportion (3 males per female) is unlike other Anthidiini bees (Anthidium florentinum, Fortunato et al., 2013).

PLANT VISITATION AND POLYLECTY

Our results indicate low specificity of R. sticticum for particular plant species, in concordance with previous studies (Bosch et al., 1993; Aguib et al., 2010; Torné-Noguera et al., 2014). Specificity of bees to special feeding plants has been described as a rare phenomenon (Cane & Sipes, 2006; González-Varo et al., 2016). Indeed, R. sticticum appears to be a polylectic bee (Bosch et al., 1993; Müller, 1996), although it probably has a preference for bee-specialized (melittophilous) plants, such as Antirrhinum, Linaria and Papillionaceae (Blanco-Pastor et al., 2015; Vargas et al., 2017), and for deep-corolla flowers, like the Labiatae (Appendices 1–2). The flowers of melittophilous plants show fusion of petals (sympetaly) and a bipartite perianth that hinders the entrance of insects other than bees and other Hymenoptera (Vargas et al., 2010; Blanco-Pastor et al., 2015). This flower structure protects the floral reward, thus ensuring that individuals reaching the bottom of the flower will most certainly get it, a reason why it could be so appreciated by R. sticticum females. It is particularly noteworthy the interest showed by R. sticticum in Antirrhinum species all through its range (see Appendices 1–2), proving that it is not a local preference, but a general one.

FLIGHT ABILITY

Flight ability by R. sticticum is identical to that described for R. septemdentatum (Nachtigall, 1997a). It is fast and precise and could be hypothesized that its good sight is, in part, responsible for it. Very few and recent studies concerning sight and perception have been performed on solitary bees (Loukola et al., 2020), but multiple discoveries in bumblebees confirmed learning skills, precise colour and shape discrimination (Giurfa et al., 1995; Spaethe et al., 2001; Dyer & Chittka, 2004; Solvi et al., 2020). The exploratory behaviour observed in R. sticticum males (and probably females, though it was not detected) is very similar to that described by Loukola et al. (2020) in Osmia bees when searching for suitable nesting sites.

TERRITORIALITY AND MATING

Rhodanthidium sticticum males, like most Anthidiini bees, are usually larger than females (García-González & Ornosa, 1999; Michener, 2007; Erbar & Leins, 2017), a probable consequence of territoriality, which helps them to get and defend better territories (Severinghaus et al., 1981; Villalobos & Shelly, 1991). Defence of territory is widely spread among Anthidiini (Michener, 2007). Selection of territories where deep-corolla flowers are predominant has been previously reported for Anthidium maculosum (Alcock et al., 1977), A. septemspinosum (Sugiura, 1991), Anthidiellum notatum and A. perplexum (Turell, 1976). Deeper corollas difficult females from seeing nearby males and escaping them. In the closely related species R. siculum, however, the defended territory is not rich in feeding flowers, but in empty shells for nesting (Erbar & Leins, 2017). In this case, R. siculum males take advantage of females when they are inside the shells. Despite the abundance of deep-corolla flowers, many attempts at copulation were unsuccessful, due to the lack of receptiveness and the ready flight of the females, just like in other Anthidiini bees (Wainwright, 1978; García-González & Ornosa, 1999; Erbar & Leins, 2017).

In the case of R. sticticum, the fierce defence is oriented not only against other males, but also against individuals from other species. This behaviour has also been described for A. florentinum, against much bigger Xylocopa violacea bees (García-González & Ornosa, 1999), for A. maculosum against hawkmoths (Alcock et al., 1977) or for A. palmarum against Anthophora bees (Wainwright, 1978). A different behaviour is showed by Anthidiellum notatum and A. perplexum, smaller Anthidiini that do not strike the intruders, but just chase them until they leave the territory (Turell, 1976). On the other extreme are Anthidium manicatum, whose males bear long spines at the end of the abdomen which they use to hurt or even kill intruders (Wirtz et al., 1988), and R. septemdentatum (Nachtigall, 1997b), that attacks the wings of the intruders. That extremely aggressive behaviour was not observed in R. sticticum, but it could not be discarded. Interspecific territoriality as shown by R. sticticum and the other species has been described as a way of keeping competitors of females (for nectar and pollen) away and maintaining the attractiveness of the territory (Severinghaus et al., 1981; Wirtz et al., 1988).

The fact that some males enter the alleged territories of other males may indicate several things: territories overlap, new or young males looking for a territory, or opportunistic wandering males, without a territory. The presence of wandering males was described in A. florentinum (García-González & Ornosa, 1999), A. maculosum (Alcock et al., 1977), A. manicatum (Severinghaus et al., 1981), A. septemspinosum (Sugiura, 1991) and R. siculum (Erbar & Leins, 2017), fighting because of territories overlapping was described for A. banningense (Jaycox, 1967) and territories changing ownership was described for A. manicatum (Severinghaus et al., 1981). The three causes seem to be plausible for R. sticticum, but further observations including individuals measuring and marking should be done to confirm it.

Unlike most bees, Anthidiini females are polyandrous, whereas males exhibit resource defence polygyny (Michener, 2007). In this context, it has been demonstrated that, in A. manicatum, the last copulating males have an above-average chance of fertilizing the female’s egg (Lampert et al., 2014), and the same has been theorized for A. florentinum (García-González & Ornosa, 1999). The polyandrous behaviour of R. sticticum females, together with the polygyny by males, could be driven, as it happens in A. manicatum and most certainly in A. florentinum, by spermatic competence.