Aleuroclava aucubae (Kuwana, 1911)

Gavrilov-Zimin, I. A. & Borisov, B. A., 2020, Aleuroclava aucubae (Homoptera: Aleyrodinea), a new adventive species for Russian Black Sea Coast, and its concomitant entomoparasitic fungus Conoideocrella luteorostrata (Ascomycota: Hypocreales: Clavicipitaceae), Zoosystematica Rossica (Zoosyst. Rossica) 29 (1), pp. 3-10 : 4-8

Aleuroclava aucubae (Kuwana, 1911)

( Figs 1–3 )

Material examined. Russia, Krasnodar Terr., Black Sea Coast of Russian Caucasus , Sochi National Park , Agur Gorge , 43°33′18″N, 39°48′15″E, 120 m altitude, on lower side of leaves of Ficus carica and Ulmus glabra , 13.X.2019 (B.A. Borisov leg.).

Description. Ultimolarva (pseudopupa) black, with fine secretions of white wax along midline, longitudinal and transverse moulting sutures. Body broadly oval, tapered posteriorly, about 0.8 mm long and 0.5 mm wide; body margin slightly jagged. Vestigial legs and antennae of usual size and shape for larvae of Aleyrodidae . Anal (vasiform) orifice cordate in form, about 25 µm in inner diameter, with strongly sclerotised margins and with notch on posterior margin. Anal operculum large, totally covering lingula. Anal (caudal) furrow well developed, about 75 µm long. Clearly visible pair of tracheal notches present on margin of prothorax. Submargin separated from dorsal disc by suture. Abdominal part of dorsal disc with characteristic “trilobite-like” sclerotisation. Glandular areas of irregular shape and size present along midline on dorsum and forming two symmetrical longitudinal rows in submedial zone of dorsal disc. Minute tubular wax glands, each about 5 µm long, sparsely scattered on all dorsal surface of body. Setae of dorsal disc forming one pair in anterior part of body, one par near transverse moulting suture and one pair near anal apparatus. Caudal setae two in number, each about 75 µm long. Ventral setae forming two symmetrical pairs on last abdominal segments.

Imago and larvae of other instars not found.

Mode of life. Similar to other species of Aleyrodinae, A. aucubae has a life cycle including a mobile primolarva with well-developed legs and antennae and three immobile larval instars, bearing vestigial poorly visible appendages ( Fig. 4 ). An ultimolarva (IV instar) is often incorrectly named “puparium” in the applied and even in the fundamental literature on whiteflies. Meanwhile, in classical entomological literature, the real puparium is represented by larval exuviae covering the pupa, a quiescent instar which moults into imago (for example, in Diptera – Cyclorrhapha and Strepsiptera). To the contrary, there is no pupa inside of ultimolarval exuviae of whiteflies; the imaginal cuticle is forming just under the larval cuticle ( Weber, 1934; Kluge, 2010; Gavrilov-Zimin, 2018). Thus, the preimaginal instar of whiteflies may be correctly named as ultimolarva ( Kluge, 2010) or pseudopupa. All larvae of whiteflies, including A. aucubae , are obligatory associated with their host plants. At the same time, winged imago can easily change their host plants; after mating, the females lay and attach eggs on the plant surface (usually a lower surface of leaves). A primolarva searches suitable place on the leaf surface for feeding and then inserts its stylets into the plant tissue. After the first moulting, the larva loses normally developed legs and antennae and looks like a flat oval scale, often covered with quaint wax secretion.

The species is polyphagous and it was reported from different countries on the plants from the families Aquifoliaceae , Araliaceae , Caprifoliaceae , Cornaceae , Flacourtiaceae , Juglandaceae , Lauraceae , Moraceae , Oleaceae , Pittosporaceae , Rosaceae , Rubiaceae , Rutaceae , Theaceae , and Ulmaceae . In Western Europe, the most usual host plants are different species of the genera Citrus , Prunus and Ficus . In the Russian Black Sea Coast area, specimens of A. aucubae were found in large colonies on Ficus carica ( Moraceae ) which is an aboriginal plant for the region and common in the lowlands as well as in the foothills along river gorges and on rocks ( Timukhin, 2006). Smaller colonies were also discovered in the same place on leaves of Ulmus glabra ( Ulmaceae ).

Distribution. China, Japan. Adventive for South Europe ( France, Italy, Slovenia, Croatia, Montenegro), Russia (Krasnodar Territory), Azerbaijan, and USA.

Ecological association with an entomoparasitic fungus. A new adventive whitefly species, Aleuroclava aucubae , was collected in a course of longterm survey of entomoparasitic fungi, conducted by the second author in different parts of European Russia and especially in the Black Sea Coast of Caucasus. Six years ago, the tropical fungus Conoideocrella luteorostrata was found for the first time in the European part of Russia in Sochi Region (Agur Gorge), as associated with the whitefly Aleyrodes sp. which was feeding on leaves of Salvia glutinosa ( Lamiaceae ). In subsequent years, the fungus was collected in other humid gorges on the territory of Sochi National Park, as well as in the Yew and Boxwood Grove (Caucasus Nature Reserve), where the fungus was found on a western red scale, Chrysomphalus dictiospermi (Morgan, 1889) (Diaspididae) , feeding on the leaves of Hedera colchica ( Araliaceae ) ( Borisov, 2017). The infected insects demonstrate a very characteristic appearance, they resemble round velvety “wart”, about 2–6 mm in diameter, of white, yellow, orange, pink, brownish colour, depending of the age of the mycelium ( Fig. 5 ). The same fungal bodies were again found in October 2019 in the Agur Gorge of the Sochi National Park, firstly on the leaves of Salvia glutinosa , and then also on the leaves of Ficus carica . Only later, numerous minute ultimolarvae of A. aucubae (both infected and not infected) were detected and collected for the laboratorial studies.

Conoideocrella luteorostrata is widely distributed in wet tropical and subtropical regions of the world: South and Central America, Mex ico, Southern USA (Florida), equatorial Africa ( Ghana), Japan, Thailand, Sri-Lanka, Indonesia, Seychelles, Samoa, and New Zealand, where it is a parasite of different scale insects and whiteflies ( Hywel-Jones, 1993; Saito et al., 2012). C. luteorostrata was first reported from Russia in 1950s from two localities in the Far East (Amur Province) as associated with an armored scale insect, Lepidosaphes ulmi (Linnaeus, 1758) ( Diaspididae ), ( Koval, 1984). Then, it was found in 1993 on the Kuril Islands as associated with another armored scale insect, Kuwanaspis sp. ( Diaspididae ), feeding on the leaves of Sasa kurilensis ( Poaceae , Bambusoideae) ( Borisov, 2017). In 2015–2016, the fungus was unexpectedly discovered in one locality of the Moscow Province ( Russia) on a whitefly, Aleyrodes asari (Schrank, 1801) , feeding on the leaves of Asarum europaeum ( Aristolochiaceae ) ( Borisov, 2017). C. luteorostrata always inhabits very humid habitats and it could be used for decreasing the number of the injurious whiteflies and scale insects in humid conditions only. For example, Saito et al. (2012) considered C. luteorostrata as a promising agent for biological control of the populations of Aleurocanthus camelliae Kanmiya et Kasai, 2011 ( Aleyrodinea ), injuring humid tea plantations in Japan.

Figures

Fig. 1. Morphology of the prepared ultimolarva (pseudopupa) of Aleuroclava aucubae, dorsal and ventral surfaces.

Fig. 2. Photo of the microscopic slide with an ultimolarva (pseudopupa) of Aleuroclava aucubae.

Fig. 3. A colony of ultimolarvae (pseudopupae) of Aleuroclava aucubae on leaves of Ficus carica, and a separate ultimolarva enlarged.

Fig. 4. A generalised scheme of ontogenesis in whiteflies.

Fig. 5. Ultimolarvae of Aleuroclava aucubae, infected by Conoideocrella luteorostrata.