Paravespa (Paravespa) rex

Fateryga, Alexander V. & Ivanov, Sergey P., 2013, Nesting biology of Paravespa rex (von Schulthess 1924) (Hymenoptera: Vespidae: Eumeninae) in the Crimea, Ukraine, Zootaxa 3721 (6), pp. 589-600 : 590-597

Paravespa (Paravespa) rex (von Schulthess in Friese & von Schulthess 1924)

Odynerus (Hoplopus) rex von Schulthess in Friese & von Schulthess 1924: 285, ♀, ♂ (type locality: “Turkestan, Kisilkum” [ Uzbekistan]).

Odynerus (Hoplopus) rex var. clarior von Schulthess in Friese & von Schulthess 1924: 285, ♀, ♂ (type locality: Kyzyl-Kum), synonymized by van der Vecht & Fischer 1972.

Odynerus (Hoplopus) rex var. obscurior von Schulthess in Friese & von Schulthess 1924: 285, ♀ (type locality: Kyzyl-Kum), synonymized by van der Vecht & Fischer 1972.

Hoplomerus jakobsoni Białynicki-Birula 1926: 893 , ♀ (type locality: boundary between the Kyzyl-Kum desert and Golodnaya steppe near Syr-Darya River), synonymized by Blüthgen 1939.

Paravespa regina Blüthgen 1939: 258 (invalid emendation).

Paravespa rex var. rufina Blüthgen 1955: 10 , ♀ (type locality: steppe between Syr-Darya and Tashkent), synonymized by van der Vecht & Fischer 1972.

Paravespa rex var. submimetica Blüthgen 1955: 11 , ♀ (type locality: Kyzyl-Kum), synonymized by van der Vecht & Fischer 1972.

Hoplomerus rex: Kostylev 1928: 399 , Crimea, “Tukluk” [Bogatovka].

Paravespa rex: Kurzenko 1977: 678 , Crimea (vicinities of Sudak, Karadag).

Paravespa rex: Fateryga & Ivanov 2010: 187 , Crimea (“Tukluk” [Bogatovka], Karadag, Lis’ya bay).

Material examined. Ukraine, the Crimea: 1 ♀, the vicinities of Sudak, “Tukluk” (= Bogatovka) (44°52'N 35°3'E), 20.VI–3.VII.1922, leg. V. Wuczeticz (ZMMU); 1 ♂, Karadag (44°55'N 35°12'E), 4.VII.1928, leg. G. Kostylev (ZMMU); 1 ♀, 3 ♂, Lis’ya bay (44°54'N 35°9'E), 13.VI.1995, leg. S. Ivanov (VTNU); 1 ♀, ibid., 13.VI.2007, leg. A. Fateryga (VTNU); 1 ♂, ibid., 5.VI.2008, leg. A. Djaparov (VTNU); 1 ♂, ibid., 26.VI.2009, leg. A. Fateryga (VTNU); 3 ♂, ibid., 12.VI.2010, leg. A. Fateryga (VTNU); 1 ♂, ibid., 15.VI.2011, leg. A. Fateryga (VTNU); 1 ♀, ibid., 16.VI.2011, leg. A. Fateryga (VTNU); 1 ♂, ibid., 2.VII.2011, leg. A. Fateryga (VTNU); 1 ♂, south slope of Echkidag (44°54'N 35°8'E), 20.VI.2009, leg. K. Shorenko (VTNU).

Distribution. Ukraine (Crimea), Turkey, Iran, southeastern Kazakhstan, Kyrgyzstan, and Uzbekistan (Giordani Soika 1970; Kurzenko 1977; Ebrahimi & Carpenter 2008; Yildirim & Gusenleitner 2012). In the Crimea this species is distributed on the South Coast between city Sudak and Karadag Nature Reserve (Fateryga 2010).

Natural history. Nesting substrate. Females of Paravespa rex made their nests on both horizontal and sloping ground surfaces. The nesting substrate at the first and the second nesting sites near the sea coast was flat proluvial terraces formed by the ground, which had been washed off from nearest badland slopes. This proluvial sediment covered the parent material of the terraces with a 10–12 cm layer of clay loam. The nesting substrate on the badland slope was deluvial aprons formed by similar clay loam but with small stone conglomeration inclusions. A total of 30 nests were observed on the proluvial terraces and 12—on the deluvial aprons.

The soil formed at all nesting sites was bluish-grey carbonate clay loam of different densities. The middle loam was formed at the first site near the sea coast; the dense one—at the second site near the sea coast and at the site on the badland slope ( Table 1 ). The greater content of physical clay parts at the site on the badland slope can be explained by mixing of the clay with the dust from a neighboring road at two other sites. Thus, the substrate at the sites near the sea coast had a dual origin. The first nesting site near the sea coast was closer to the road than the second one; thus, the substrate at the first site was more mixed and contained less physical clay.

The surface of the ground nearly lacked vegetation at the nesting sites of P. re x. Only a few clumps of Camphorosma monspeliaca L. ( Chenopodiaceae ) and several herbs of Galatella villosa (L.) Rchb. f. ( Asteraceae ), Ceratocarpus arenarius L. ( Chenopodiaceae ), and Allium paczoskianum Tuzson (Amaryllidaceae) with total coverage about 1–3% were found at the sites near the sea coast. Several climbers of Capparis herbacea Willd. (Capparaceae) grew in addition to aforesaid species on the site at the badland slope.

Nest-building and hunting activity. The activity period of the females of P. re x began at 7.40 and finished at 18.00–18.30 ( Fig. 7 ). Females started their nesting by searching for a place for the nest 18–40 min. ( Table 2 ). After the place had been chosen, they went for water. Females collected water on banks of the streamlet ( Fig. 3 ), at puddles, and rarely on the seashore. The duration of the flights could be very different due to the situation at the water-collecting site. If females had been not disturbed by humans they arrived after less than one minute. In the opposite case they could be absent for several minutes.

Duration of excavation of the nest burrow and the first cell 3 125–148 135.3±6.8 (including the duration of the construction of the turret) (min)

Duration of a flight for water (sec) 55 43–409 103.5±10.1 Number of flights for water during the excavation of the nest 3 23–28 26.0±1.5 burrow and of the first cell (including the construction of the

turret)

Duration of sealing of the cell and excavation of the next (min) 3 81–111 94.7±8.5 Number of flights for water during the sealing of the cell and the 3 10–16 12.7±1.7 excavation of the next

Duration of the sealing of the nest (min) 3 25–31 27.7±0.7 Number of flights for water during the sealing of the nest 3 6–7 6.3±0.3 A female returned to the nesting site with the water in her crop and regurgitated it onto the ground surface. After that, she began to excavate a vertical nest burrow and to construct the turret at the same time. She mixed mortar with water and soil, formed mud pellets, retrieved them from the nest burrow, and laid them around its entrance. After each mud pellet had been laid, she smoothed its inner surface with her mouthparts. She held on the inner surface of the turret with her forelegs and on the outer one—with the middle and hind legs ( Fig. 4 ). In this way, the turret grew upwards and the burrow grew downwards at the same time.

The turrets of the nests of P. re x were 2–3.5 cm tall and about one cm wide and had two distinct architectural forms: funnel-shaped and curved ( Figs 5, 6 , 8 ). The duration of the construction of the turret was 18–55 min. ( Table 2 ) due to its form. Funnel-shaped turrets were made longer than curved ones. Among the observed nests, 11 nests had funnel-shaped turrets and 31 curved ones.

After the turret had been completed, the female continued the excavation of the nest burrow. At this time she also retrieved similar mud pellets from the nest. However, she did not use them for turret but flew from the nest for few seconds, and dropped them away. It is interesting, that each female had only a few places where she dropped the pellets. One female dropped them strongly at two places: on the shadow of an oleaster tree, Elaeagnus angustifolia L. ( Elaeagnaceae ) grown near the nesting site ( Fig. 1 ) and into a cup that stood near one of the observers. Another female dropped mud pellets at three places: into bushes in the gully bottom near the nesting site and onto both observers who sat at opposite directions from her nest.

Females flew for water during the whole period of the excavation of the nest burrow, as well as during the construction of the turret. Each portion of water could be used for making 2–6 mud pellets and dropping them away or using them for the turret. Thus, females flew for water 23–28 times during this stage of the nest-building works lasted 125–148 min. ( Table 2 ).

After the nest burrow 10–12 cm deep had been completed, females laid an egg and flew for hunting. Females hunted for caterpillars on the phrygana and steppe slopes not far from the nesting sites. The duration of the flights for hunting varied due to hunting success. If hunting was not successful, females several times returned to their nests without prey and flew again. The duration of the packing of a caterpillar into the cell varied also very much ( Table 2 ), because sometimes females simply laid it inside the nest, and sometimes they rearranged also the other caterpillars, which were already available in the cell. The number of caterpillars stored in one cell was 3–7 (mean—3.7±0.5; N =7).

After the provisioning, females sealed the cell with a mud plug and excavated the next cell or sealed the nest. If a female sealed the cell and excavated the next one, only mud excavated from the next cell was used for the cell plug. In this case, the excess mud pellets were dropped after the cell sealing in the way described above. If a female sealed the cell and the nest, she used only the material of the turret. She flew for water and then regurgitated it onto the top of the turret. Then, she became to make a mud pellet with her mouthparts, held on the turret by all of her legs ( Fig. 6 ). After that, she took the pellet with forelegs and came down into the nest. These actions were repeated several times and interrupted only by flights for water. The durations of the sealing of the cell and the excavation of the next one and of the sealing of the nest as well as the numbers of flights for water during these actions are presented in Table 2 .

The chronogram of the activity of three females of P. re x during one day (14.VI.2010) is represented in Fig. 7 . It shows all flights of the females from the nests and all their arrivals, except the flights for dropping of the mud pellets, which were too short to show them on the chronogram ( Table 2 ). Three females (A, B, and C) started their day nearly at the same time. Females A and C continued the provisioning started yesterday and female B started with laying of an egg and provisioning of a new cell built yesterday. In the afternoon females A and C had completed provisioning and started sealing their cells and excavation of the next ones in the same nest burrows. After that, these females laid their eggs and started provisioning, which was finished with more or less success at 18.00 (female A) or 18.30 (female C). Female B completed and sealed her nest in the afternoon and started a new nest after 15.00. The excavating works of this female lasted up to 18.00. Thus, one female of P. re x can build and provision somewhat less than two cells per day, if the weather is favorable.

Structure of complete nests. The nests of P. re x contained 1–3 cells (mean—1.9±0.2; N =11) disposed vertically or slightly inclined ( Fig. 9 ). The depth of the nest burrows with the cells was 10–12 cm. Thus, the nests were excavated exactly at the lower border of the proluvial sediment of clay loam at the nesting sites near the sea coast. The substrate suitable for the nests at the site on the badland slope was significantly deeper, but the nests studied there had the same dimensions. Each cell in the nests was sealed by separate mud partition; similar partitions were found in the other parts of the nest burrows. The nest burrows were not filled with mud because only turret material had been used by females to seal the nests (see above). The nest plug was thicker than the other partitions and towered for 1–2 mm above the ground surface ( Figs 9 , 12 ). An uncompleted nest plug was found in one nest left by female after human disturbance ( Fig. 9 A).

The inner surface of the nest burrows and the cells was very smooth and polished by the females. In freshly excavated burrows it was also wet and lustrous. The nest and cell plugs, partitions in the nest burrow as well as its walls and the turrets were easily destroyed by rain. Females repaired their nest burrows and made new turrets after rains. However, the rain water penetrated also to already sealed nests and caused a rotting of the provisions (see below).

Immature instars and development. The egg of P. re x was laid by the female into the freshly excavated cell before provisioning. It was stood vertically onto the cell bottom ( Fig. 10 ) without any attaching adhesive material or filament (four eggs of four different females were observed). The egg was only stuck with its posterior end to the bottom of the cell due to its wet surface. After the first prey had been stored into the cell and touched the egg, it fell. However, the egg remained in a more or less vertical position because the first caterpillar was stored around it. The size of the egg was about 3× 1 mm.

The larva hatched from the egg began feeding on the second caterpillar stored in the cell above the anterior end of the egg. After consuming of all provisions, it spun a cocoon. The cocooning began with storing prey remains and their feces at the top of the cell. These waste products were separated from the remaining part of the cell with multilayered part of the cocoon, with thin yellowish layers. After that, the larva constructed the thick part of the cocoon covering the bottom of the cell and its lateral walls. This part was made with the help of fluid secretion penetrating into the cell walls and making them durable and water-proof. After the construction of the cocoon, the meconium was discharged onto the bottom of the cell and spread all over it. Then, the larva transformed into the prepupal stage and became coiled. The inner volume of the cocoon significantly exceeded the size of the prepupa ( Fig. 11 ). Durations of the egg, feeding and cocooning stages were not measured.

Hibernation occurred at the prepupal stage. After the winter diapause the prepupa unrolled and became straight. Pupation occurred 10 days after unrolling; the pupa developed over 19–21 days. Six prepupae were obtained in 2010 and observed. One female and one male emerged in June, 2011, and one female and one male emerged also in June, 2012. The fifth prepupa hibernated three years running and a male emerged from it in June, 2013. The sixth prepupa was also alive in 2013 and obviously remained in a four-year diapause. It is interesting that one of the wasps emerged in 2011 was from the same nest as one of the wasps emerged in 2012.

The observations showed that P. re x is univoltine species with very short flight times. Wasps of both sexes were recorded from 1.VI to 4.VII. Females started their nesting during the middle of the first 10 days of June and usually finished it the last week of the month.

Trophic links. Females of P. re x hunted exclusively for caterpillars of noctuid-moths of the genus Heliothis Ochsenheimer ( Lepidoptera : Noctuidae ) ( Fig. 13 ). Females collect them on inflorescences of the sickle alfalfa plants, Medicago falcata L. ( Fabaceae ) grown in abundance not far from the nesting sites. The hunting was not observed, but the inspecting flights of the wasp females were registered only around the plants of this species. Moreover, the caterpillars found feeding on this plant were identical to the caterpillars from the wasp cells. Two species were recognized among them; the first one, Heliothis peltigera (Denis & Schiffermüller) had been reared to imago and was identified without doubt. The second species was not reared, but presumably it was H. viriplaca (Hufnagel) .

Adult feeding was observed only on flowers of Thymus tauricus Klokov & Des. -Shost. ( Lamiaceae ) ( Fig. 14 ), mainly in the late afternoon. Three males and one female were recorded on the flowers at 16.30–16.40; however, one female was recorded at 12.45.

Parasites, associates and reproductive success. The chrysidid wasp Chrysis valesiana Frey-Gessner (Chrysididae) was the only parasite closely associated with the nests of P. re x. Its cocoons were found among a large amount of prey remains in four wasp cells. It was impossible to ascertain whether it fed on prey or on the wasp larvae. Females of Ch. valesiana were observed several times when they entered the nests of P. re x at provisioning stages. Another chrysidid wasp, Hedychrum virens Dahlbom as well as its host, Cerceris tuberculata de Villers ( Crabronidae ) were observed entering one nest of P. re x one after another. Apparently, they entered to the nest by mistake, because the nest of C. tuberculata was 50 cm from the nest of P. re x.

Workers of the ant Cataglyphis aenescens (Nylander) (Formicidae) were also observed disturbing the nesting females of P. re x. They attacked the females and stole portions of the water which had been regurgitated by wasps to make a mortar. However, such behavior of the ants was observed only at two stages of the nest-building: at the beginning of the excavation of the nest burrow and at the ending of the sealing of the nest. At the other periods of the nesting, when the nest turret was more than one cm high, the ants never attacked the wasps.

The reproductive success of P. re x was not high. Only 12 nests (28.6%) were successful among 42 observed ones. The other nests were left by the females at the times of the excavation of the burrow before egg laying and provisioning. Seven abandoned nests were dissected. Three of them were left because the female had found an obstacle blocking the nest burrow. It was small stones in two nests or a cigarette filter in another one. Three other nests were left because the females had been disturbed by humans. One nest was left for no visible reason.

Eleven successful nests with 21 cells were examined. Seven cells (33.3%) were successful; four cells (19.0%) were damaged by Ch. valesiana , and 10 cells (47.6%) by rain. The water had penetrated into these cells at the egg or feeding larva stages before the water-proof cocoon was spun.

The burrows of four abandoned nests of P. re x were occupied by nests of two species of megachilid-bees ( Hymenoptera : Megachilidae ): Anthidium cingulatum Latreille (three nests) ( Fig. 15 ) and Hoplitis jakovlevi (Radoszkowski) (one nest).

Male behavior. Males spent most their time near the water sources. They made patrolling flights along the streamlet and the seashore or around the puddles where the females were collecting water. Sometimes males sat on stones waiting for females ( Fig. 16 ). Males were observed attacking water-collecting females many times, but the courtship was observed only once. The male sat atop the female and began to stimulate her with antennae and with the top of his abdomen ( Fig. 17 ). These actions lasted nearly 20 min. until the male saw another female searching for caterpillars on the sickle alfalfa plant. The male left the first female and flew after the second one. Copulation was not observed.

Figures

FIGURE 7. Chronogram of the activity of three females of Paravespa rex during one day (14. VI. 2010). A. First female; B. Second female; C. Third female.

FIGURES 1 – 6. Nesting biology of Paravespa rex. 1. First nesting site near the sea coast; 2. Nesting site on the badland slope; 3. A female collecting water from the streamlet; 4. A female constructing curved turret; 5. Funnel-shaped turret; 6. A female demolishing curved turret.

FIGURES 8 – 11. Structure of nests and cells of Paravespa rex. 8. Two types of nest turrets of P. re x, lateral view (A, funnelshaped; B, curved); 9. Plans of complete nests of P. re x, lateral view (A, nest with one cell lost by female at the time of its sealing; B, nest with two cells; C, nest with three cells); 10. Position of the egg in the empty cell; 11. Position of the prepupa inside the cocoon in the sealed cell (A, mud plug of the cell; B, prey remains; C, prey feces; D, multilayered part of the cocoon; E, thick one-layered mud-containing part of the cocoon; F, meconium).

FIGURES 12 – 17. Nesting, feeding, and mating behavior of Paravespa rex. 12. Plug of the freshly sealed nest; 13. Caterpillars of Heliotis spp. recovered from two nest cells; 14. Male feeding on Thymus tauricus flowers; 15. Abandoned nest occupied and sealed by Anthidium cingulatum; 16. Male guarding on a stone near the streamlet; 17. Courtship.

Tables

TABLE 1. Parameters of the soil substrate containing the nests of Paravespa rex at three nesting sites.

Nesting site	Density (g/cm3)	Content of physical clay— Granulometric class parts <0.01 mm (%)
First site near the sea coast	2.70	36.56 Middle clay loam
Second site near the sea coast	2.54	49.32 Dense clay loam
Nesting site on the badland slope	2.66	60.16 Dense clay loam

TABLE 2. Nesting and hunting activity of the females of Paravespa rex.

Parameter	N	Minimum–maximum Mean±SE
Duration of searching for a place for the nest (min)	3	18–40 31.0±6.4
Duration of construction of the turret (min)	3	18–55 42.7±11.9