Celonites tauricus Kostylev, 1935

Fateryga, Alexander V., Mauss, Volker & Fateryga, Valentina V., 2022, New distributional records of Celonites tauricus (Hymenoptera, Vespidae, Masarinae) and new data on its behaviour at flowers, Journal of Hymenoptera Research 92, pp. 241-256 : 241

Celonites tauricus Kostylev, 1935

Celonites abbreviatus tauricus Kostylev, 1935: 108, [♀]. Type locality: “Крым” [Crimea]; neotype (designated by Mauss et al. 2016), ♀ (dbM 4305): Crimea, vicinity of Feodosiya, Lisya Bay, 16.06.2010, A. Fateryga (OLML).

Celonites spinosus Gusenleitner, 1966: 359-362, ♀ ♂. Type locality: “Kusadasi” [Turkey]; holotype, ♀ (dbM 4665): Turkey, Kusadasi, 11.06.1964, J. Gusenleitner (JG). Synonymized by Mauss et al. (2016).

Celonites abbreviatus invitus Gusenleitner, 1973: 58-59, ♀ ♂. Type locality: “Türkei, Gürün” [Turkey]; holotype, ♀ (dbM 4662): Turkey, Gürün, 05.06.1970, J. Gusenleitner (JG). Synonymized by Mauss et al. (2016).

Material examined

(new records). Greece: Chios: Spartounta, 38.5428°N, 25.9964°E, 13.06.2007, 1 ♀ (dbM 5353), leg. A. Ebmer [OLML]; W Pyrgi, Kato Fanou , 38.2219°N, 25.9672°E, 12.06.2007, 3 ♀ (dbM 5354-5356), leg. A. Ebmer [OLML] ; Rhodes: Kolymbia, Akra Vagia , [36.2536°N, 28.1759°E], 29.05.2005, 1 ♂ (dbM 5181), leg. B. Tkalců & O. Tkalců [OLML] ; Samos: Mt. Kerkis, NE shoulder, [37.7490°N, 26.6406°E], 08.07.1994, 1 ♀ (dbM 5357), leg. A. Ebmer [OLML]; Mt. Kerkis , S shoulder, [37.7182°N, 26.6250°E], 11.07.1994, 4 ♀ (dbM 5358-5361), leg. A. Ebmer [OLML] . Russia: Dagestan: [Makhachkala urban okrug], vicinity of Talgi, 42.8767°N, 47.4451°E, 25.06.2018, 1 ♂, leg. Yu. Astafurova, K. Fadeev, V. Loktionov, M. Mokrousov & M. Proshchalykin [AF]; ibid., on Teucrium canum , 12.06.2019, 2 ♀, 1 ♂, leg. A. Fateryga [AF], 1 ♀ (dbM 5511), 1 ♂ (dbM 5510), leg. A. Fateryga [VM], 13.06.2021, 1 ♀, leg. A. Fateryga [AF], 18.06.2021, 1 ♀ (dbM 5998, BOLD process ID CECYP021-22), leg. A. Fateryga [VM]; Crimea: [Yalta urban okrug], Miskhor, [44.4289°N, 34.0855°E], 01.08.1887, 1 ♀ [ZISP]; Sudak urban okrug, Cape Meganom [44.7940°N, 35.0815°E], 27.05.2016, 1 ♂, leg. A. Fateryga [AF]; ibid., on Ziziphora taurica , 27.05.2016, 1 ♀, leg. A. Fateryga [AF]; Feodosiya urban okrug, Lisya Bay , [44.8983°N, 35.1575°E], 22.06.2016, 1 ♂, leg. A. Fateryga [AF] . Georgia: Kasbek , [42.6950°N, 44.5147°E], 1 ♀ [ZISP] . Armenia: [Armavir Province], Parakar , [40.1665°N, 44.4070°E], 02.05.1925, 1 ♀, [leg. M. Rjabov] [ZMMU, on loan in AMNH] . Azerbaijan: [Masally District], Zuvand , [39.0048°N, 48.4771°E], 08.06.1985, 1 ♂, leg. V. Tobias [FSCV] . Turkey: Ankara Dikmen , [39.8650°N, 32.8570°E], 05.07.1959, 1 ♀ (dbM 5652), leg. K. Guichard [MSNVE] . Cyprus: Ca. 5 km N Lemithou, Pinus-Zone, 34.9689°N, 32.8075°E, 15.06.2013, 1 ♀ (dbM 5348), leg. A. Ebmer [OLML]; Troodos, Mt. Olympos N, Pinus-Zone, 34.9289°N, 32.8703°E, 10.06.2013, 1 ♀ (dbM 5347), leg. A. Ebmer [OLML]; Troodos, Mt. Olympos N, Pinus-Zone, 34.9417°N, 32.8703°E, on Nepeta troodi , 11.06.2013, 1 ♀ (dbM 5346), leg. A. Ebmer [OLML]; Mt. Troodos , [34.9234°N, 32.8808°E], 28.06.1937, 1 ♀ (dbM 5622), leg. G. Mavromoustakis [MSNVE]; ibid., 12.08.1948, 1 ♀ (dbM 5620), leg. G. Mavromoustakis [MSNVE]; ibid., 02.08.1965, 1 ♀ (dbM 5621), leg. G. Mavromoustakis [MSNVE]; Troodos, S of Mt. Olympos, [34.9319°N, 32.8683°E], 07.07.1987, 1 ♀ (dbM 5345), leg. A. Ebmer [OLML]; Troodos, S of Mt. Olympos, Sun Valley, [34.9319°N, 32.8683°E], 10.07.1987, 5 ♀ (dbM 5340-5344), leg. A. Ebmer [OLML]; ibid., 15.07.1987, 2 ♀ (dbM 5338, 5339), leg. A. Ebmer [OLML] .

Distribution.

Greece (Chios, Kos, Rhodes, Samos), Russia (Dagestan, Crimea), Georgia, Armenia, Azerbaijan, Turkey, Cyprus, Syria, Iran. The species is new to Chios, Rhodes, Samos, Dagestan, Georgia, and the main portion of Azerbaijan (previous records were made from the Nakhchivan Autonomous Republic only). The examined specimen from Armenia was reported by Kostylev (1929) as Celonites abbreviatus .

Flower-visiting records.

Teucrium canum was the only plant species observed to be visited by males and females of Celonites tauricus in Dagestan (Table 1 ), while they were not recorded on three other species of Teucrium flowering at the same locality, namely Teucrium chamaedrys , Teucrium hyrcanum L. and the species known in the flora of Dagestan ( Murtazaliev 2009) as Teucrium polium L. " Teucrium polium " was previously recorded as a forage plant of Celonites tauricus in the Crimea ( Mauss et al. 2016), but it has to be noted that there is a taxonomic problem with this plant taxon. True T. polium does not occur in Eastern Europe, while the species commonly known there as " T. polium " is currently treated as Teucrium capitatum L. ( Tutin and Wood 1972; Govaerts et al. 2005-2022; Fateryga and Fateryga 2019). On the other hand, the lectotype designated for T. capitatum ( Rosúa and Navarro 1987) does not correspond very well to " T. polium " from Eastern Europe (including Dagestan and the Crimea), and seems to belong to a different taxon.

Specimens of Celonites tauricus were observed in the Crimea in 2020 at flowers of five species of Lamiaceae (Table 1 ). Two of them, that is Teucrium chamaedrys and Thymus tauricus Klokov & Des.-Shost., were previously recorded as forage plants of this wasp ( Mauss et al. 2016), while Salvia nemorosa subsp. tesquicola (Klokov & Pobed.) Soó and two annual species of Ziziphora are reported for the first time. The principal forage plant was Ziziphora taurica followed by T. chamaedrys , while visits to the remaining species were occasional.

The identity of the subspecies of Salvia nemorosa L. is also taxonomically complicated. It is generally accepted under the name " Salvia nemorosa subsp. pseudosylvestris (Stapf) Bornm." ( Govaerts et al. 2005-2022; Yena 2012) despite the fact that such a nomenclatural combination was not validly published, because Bornmüller (1907) applied it to a variety S. nemorosa β [var.] Salvia nemorosa pseudosylvestris (Stapf) Bornm. (as " pseudo-silvestris "), not a subspecies.

Behaviour of females at flowers.

The behaviour of females of Celonites tauricus at flowers of Teucrium canum in Dagestan was similar to the previously described behaviour of this species at flowers of Teucrium chamaedrys in the Crimea and at flowers of Satureja thymbra in Kos ( Mauss et al. 2016). During these flower visits, the females stood on the lower lip of a flower and took up nectar and pollen simultaneously. The proboscis was protruded deeply into the corolla tube while the female performed rapid back and forth movements of the anterior part of her body, rubbing her head over the nototribic anthers. In this manner pollen grains were removed from the pollen sacs and accumulated on frons and clypeus. Periodically flower visiting was interrupted and the pollen grains were transferred from the frons to the mouthparts by alternating brushing movements of the fore legs and the pollen was being ingested. This pollen-brushing behaviour took place either on flowers or on the ground in the close vicinity of the plants. Similar behaviour was observed in the Crimea in 2020 at flowers of T. chamaedrys and Thymus tauricus .

The behaviour of females at flowers of Ziziphora taurica was different. The behavioural sequence of such a flower visit could be usually subdivided into three phases. During the first phase, a female stood on the lower lip of a flower and performed rapid movements of her head for a very short period (not longer than a second), rubbing its anterior parts over the anthers (Fig. 2A ). In the following second phase, the female protruded her proboscis and moved her body headfirst deeply into the corolla tube so that only the posterior half of her body remained visible in outside view. During this phase, the anthers were in contact with the dorsal mesosoma and often also with the first and the second metasomal tergum (Fig. 2B ). The duration of the second phase was much longer than the first one; usually it lasted for some seconds. The third phase started, when the female retracted her proboscis and appeared outside the corolla tube again. Then she was rubbing her head over the anthers once more so that pollen accumulated on her frons (Fig. 2C ). Subsequently, the female usually performed pollen-brushing behaviour that took place on the same flower. Very often she brushed pollen from her frons while she was standing on the flower and continued to accumulate pollen on her clypeus that was still in contact with the anthers (Fig. 2D ). After that, the pollen was brushed from the clypeus to the mouthparts as well (Fig. 2E ). When the fore legs were brought between the mouthparts, the pollen was apparently ingested. After the pollen had been brushed from both the frons and the clypeus, the female sometimes repeated the rapid movements of her head, rubbing it over the anthers again, in the same way as in the first phase (Fig. 2F ). The duration of the third phase was variable depending on how many times the wasp switched her behaviour from pollen removal from the anthers to brushing the pollen grains from the frons and the clypeus, and back; sometimes this phase was the longest. At regular intervals the females interrupted flower visits and stood on the ground. During this time, they performed alternating grooming movements of the fore legs over the body including the dorsal mesosoma and metasomal terga, covered with pollen grains.

Thus, the pollen-collecting behaviour of the females of Celonites tauricus at flowers of Ziziphora taurica differs from that at flowers of Teucrium , Satureja , and Thymus in that pollen removal from the anthers and nectar uptake take place separately from each other in temporal succession. This difference is obviously caused by the flower structure of the genus Ziziphora , specifically its much longer corolla tube in comparison with that of the genera Teucrium , Satureja , and Thymus . Therefore, it is impossible for the wasps to reach the nectar with the proboscis and to make contact with the anthers with the frons simultaneously. A behavioural pattern similar to that of C. tauricus at flowers of Z. taurica is known for Celonites sibiricus Gusenleitner, 2007 at flowers of the genus Dracocephalum L. (also Lamiaceae ) which also have a long corolla tube ( Fateryga 2020). The main difference between them is that females of C. sibiricus do not return to pollen collection from the same flower after nectar uptake has been finished inside of the corolla tube.

The behaviour of females of Celonites tauricus at flowers of Salvia nemorosa subsp. tesquicola was similar to that at flowers of Ziziphora taurica in that the attempts to remove pollen from the anthers and nectar uptake also took place separately from each other in temporal succession. But in contrast, these pollen-collecting attempts by C. tauricus at S. nemorosa subsp. tesquicola usually failed. During the first phase, a female stood on the lower lip of a flower and attempted to rub over the anthers with her frons but usually she actually came into contact with the stigma instead of the anthers (Fig. 3A ). During the second phase, the female protruded her proboscis deeply into the corolla tube while she performed rapid back and forth movements of the anterior part of her body, apparently trying to rub her head over the anthers, though the head was in fact not in contact with them (Fig. 3B ). However, one female of C. tauricus was observed with yellow pollen of Salvia on the exoskeleton (well distinguishable from the white pollen of Ziziphora , the orange pollen of Teucrium chamaedrys , and the lilac pollen of Thymus tauricus ). This means that at least sometimes the pollen-collecting attempts of C. tauricus females at S. nemorosa subsp. tesquicola are successful. There was no third phase observed at flowers of this species, i.e., the wasps did not return to separate pollen-collecting attempts after nectar uptake. Flower visits to S. nemorosa subsp. tesquicola occurred only occasionally (Table 1 ), i.e., this species was not a principal forage plant. Such visits to a suboptimal plant species might be caused by the scarcity of the pollen sources, since they were observed in a locality with very low abundance of flowering plants (see above).

The behaviour of Celonites tauricus at flowers of Salvia nemorosa subsp. tesquicola was somewhat similar to that observed for the closely related Celonites abbreviatus at flowers of Salvia officinalis L. ( Schremmer 1959). In the latter case, the pollen removal from the anthers and nectar uptake also took place separately from each other in temporal succession. But in contrast to the situation in C. tauricus , the pollen-collecting attempts by C. abbreviatus at S. officinalis were always successful.

Pollen-collecting and pollen-brushing structures.

Examination of a female of Celonites tauricus under a SEM revealed that it possesses the same morphological structures for pollen-uptake and pollen-transfer that were previously described in detail for the closely related Celonites abbreviatus ( Schremmer 1959; Müller 1996). The pollen-collecting apparatus consists of specialized stiff “knobbed” setae covering the anterior surface of the head, particularly the frons and the clypeus (Fig. 4A-C ). Such a setation of the head is an apomorphic character of the members of the so-called C. abbreviatus -complex ( Mauss 2013). Pollen grains are removed from the anthers with the aid of these “knobbed” setae and accumulate between them on the front of the head. Then the pollen grains are transported towards the mouthparts with the fore legs, which bear comb-like rows of specialized, particularly strong pollen-brushing setae along the anterior margins of the inner surface of the first and the second segment of the fore tarsi (Fig. 4D-F ). Pollen grains that occasionally accumulate on other parts of the body, particularly on the dorsal mesosoma and metasomal terga, are also transferred towards the mouthparts with the help of these “combs” on the fore tarsi.

It is of note that the spherically swollen ends of the “knobbed” setae look somewhat flattened and often concave from one side in the SEM images (Fig. 4C ). Such depressions on the spherical distal ends of the setae were not reported for C. abbreviatus ( Schremmer 1959; Müller 1996) but were present in all four specimens of both species in our study and are also visible in some original SEM images provided by A. Müller from his investigation of C. abbreviatus published in 1996. These depressions may be artifacts resulting from air-drying, in which the original spherical shape of the swollen ends of the setae seems to collapse partially.

Male behaviour.

Males of Celonites tauricus were mainly observed at the site with flowering Ziziphora taurica , where they patrolled in flight along the plants or visited flowers. During flower visits they always inserted their proboscis into the corolla tube indicating the uptake of nectar. After that, they often performed pollen-brushing behaviour in the course of which the pollen grains were transferred from the frons towards the mouthparts, indicating pollen consumption as well (Fig. 3C ). Patrolling males pounced on females that were visiting flowers or standing on the ground. Successful copulation was observed five times: four times on flowers (Fig. 3D, E ) and one time on the ground (Fig. 3F ). Each time, the whole copulation lasted less than 10 s, which is similar to the documented copulation length in two other previously studied species of Celonites , namely C. abbreviatus ( Mauss 2006) and C. fischeri Spinola, 1838 ( Mauss and Müller 2014).

Figures

Figure 2. Behaviour of females of Celonites tauricus Kostylev, 1935 at flowers of Ziziphora taurica M. Bieb. in Lisya Bay (details see text).

Figure 3. Behaviour at flowers and mating of Celonites tauricus Kostylev, 1935 in Lisya Bay A, B females on flowers of Salvia nemorosa subsp. tesquicola (Klokov & Pobed.) Soo C a male on a flower of Ziziphora taurica M. Bieb. D, E copulation on flowers of Z. taurica F copulation on the ground.

Figure 4. SEM micrographs of the pollen-collecting and pollen-brushing structures of a female of Celonites tauricus Kostylev, 1935 A head in lateral view B close up of the frons (marked rectangular area in A) showing specialized stiff " knobbed " pollen-collecting setae C close up of " knobbed " setae (marked rectangular area in B) D inner surface of the left fore tarsal segments 1 - 3 E close up of the tarsomere 1 (left marked rectangular area in D) showing a comb-like row of specialized, particularly strong pollen-brushing setae along its anterior margin F the same for the tarsomere 2 (right marked rectangular area in D).