Pulvinaria urbicola Cockerell, 1893

Joshi, Sunil, 2017, First record of Pulvinaria urbicola Cockerell (Hemiptera: Coccidae) from India, with a key to the Indian species of Pulvinaria Targioni Tozzetti, Zootaxa 4236 (3), pp. 533-542 : 534-539

Pulvinaria urbicola Cockerell, 1893

Pulvinaria urbicola Cockerell, 1893: 160 ; Fernald, 1903: 140; Zimmerman, 1948: 342; Beardsley, 1966: 493; Hamon & Williams, 1948: 105; Williams & Watson, 1990: 158; Qin & Gullan, 1992: 154; Ben-Dov, 1993: 286; Tanaka & Amano, 2006: 177.

Material examined: Anand Nagar, Bengaluru , Karnataka (13.0358° N, 77.5970° E) 9 ♀ on Citharexylum spinosum (Verbenaceae), 12.x.2010, Sunil Joshi coll. ; Gutahalli, Bengaluru , Karnataka (12.9974° N, 77.5780° E) 6 ♀ on Pisonia grandis (Nyctaginaceae), 09.xii.2010, Sunil Joshi coll. ; Yelhanka, Bengaluru , Karnataka (13.1005° N, 77.5940° E) 7 ♀ on Lantana camara (Verbenaceae), 16.ii.2011, Sunil Joshi coll. ; Doddaballapur, Bengaluru , Karnataka (13.2927° N, 77.5389° E) 7 ♀ on Solanum lycopersicum (Solanaceae), 15.i.2016, B. Manjunath coll. ; Hesarghatta, Bengaluru , Karnataka (13.1500° N, 77.4900° E) 12 ♀ on Capsicum annuum (Solanaceae), 28.vii.2016, Shashikala Kadam coll.

Appearance in life ( Fig. 1 ): Eggs gleaming yellowish orange ( Fig. 1 A). As nymph grows, a dark brown stippled wavy marking develops on each side, arising from the paler anal plates; these lines diverge anteriorly and then converge toward head, enclosing a lanceolate paler patch on spinal area of dorsum ( Fig. 1 B). These darker wavy lines increase in width and cover almost whole dorsum except in median area. Body colour becoming lighter towards margin, with a darker pattern forming spurs towards outer periphery ( Fig 1 B, C, D).

Adult female elongate oval, but mature female convex dorsally ( Fig 1 E, F). Body colour varying with age and to some extent with host, but generally yellow to yellowish green with dark brownish markings on dorsum. No visible wax develops on the dorsum before oviposition. Ovipositing females become shrunken with age, becoming darker and body surface developing light wax deposits ( Fig 1 G, H). Ovisac white, straight or curved, convex dorsally, with four longitudinal ridges in median and lateral areas ( Fig 1 H, I). Forming colonies on lower leaf surface, around veins and on leaf margin ( Fig. 1 I).

Appearance of slide-mounted adult female: see Fig. 2 .

Body shape and size: Oval to broadly oval, 3.5–4.6 mm long, 2.75–3.15 mm wide, length 1.2–1.4 times its width. Anal cleft 350–450 µ m long.

Margin: Marginal setae each 22–55 µ m long, slender, straight, parallel-sided or curved, some bluntly pointed, some bifid and some fimbriate ( Fig. 2 A, Fig. 3 B); distributed as follows: 33–44 between anterior spiracular furrows, 14–18 between each anterior and posterior spiracular furrow, and 38–49 between each posterior spiracular furrow and anal cleft. Spiracular setae numbering 3 in each spiracular furrow ( Fig. 2 B, Fig. 3 C); median setae each 62–70 µ m long, 2.4–4.0 times as long as lateral setae, straight or slightly curved, bluntly pointed. Spiracular cleft sclerotization absent.

A. Marginal setae; B. Spiracular setae; C. Dermal areolation; D. Dorsal setae; E. Discoidal pores anterior to anal plate; F. Anal plate showing four apical setae; G. Anal plate with three subapical setae; H. Anal plates with two pairs of fringe setae; I. Submarginal setae; J. Ventral setae; K. Inter-antennal setae in five pairs; L. Prevulvar setae in three pairs; M. Antenna; N. Legs with tibio-tarsal sclerotization and free articulation; O. Claw without denticle, claw digitules and tarsal digitules; P. Spiracle without sclerotic plate; Q. Spiracular pores; R. Multilocular pores around anal area with seven loculi; S. Multilocular pores lateral to hind coxa with five loculi; T. Ventral tubular duct type I, present medially on head and thorax; U. Ventral tubular duct type II, present medially on abdominal segments; V. Ventral tubular duct type III, present in a broad submarginal band from anal cleft to posterior spiracle.

Dorsum: Derm membranous ( Fig. 2 C, Fig. 3 A). Dermal areolation present in submarginal area. Dorsal setae each 7–11 µ m long, spine-like, scattered ( Fig. 2 D, Fig. 3 E). Submarginal tubercles generally absent but one or two occasionally present in some specimens (present in two out of 41 specimens examined, Fig. 3 F). Disc pores not detected. Discoidal pores, each 2–3 µ m in diameter, present in group of 3–10 in median area anterior to anal plates ( Fig. 2 E, Fig. 3 G). Tubular ducts scattered ( Fig. 3 H) but most abundant in thoracic area; each duct 6-7 µ m long, 2– 2.5 µ m wide, inner filament 5–6 µ m long. Microducts ( Fig. 3 I) scattered, most numerous on mid-dorsal areas of abdomen and thorax, with inner filament 3–7 µ m long. Anal plates each triangular, each 140–176 µ m long, 76–99 µ m wide; anterolateral margin concave, 96–130 µ m long, with 4 pairs of apical, 3 pairs of subapical and two pairs of fringe setae ( Fig. 2 F, G, H, Fig. 3 J1, J2). Anal ring ( Fig. 3 K) with 8 setae; translucent pores present in 1–3 rows.

Venter: Submarginal setae each 11–16 µ m long, slender, straight, acute ( Fig. 2 I, Fig. 3 L); distributed as follows: 16–20 between anterior spiracular furrows, 4–6 between each anterior and posterior spiracular furrow, and 12–19 between each posterior spiracular furrow and anal cleft. Ventral setae, each 15–49 µ m long ( Fig. 2 J, Fig. 3 M), similar to submarginal setae. Interantennal setae numbering 4 or 5 pairs ( Fig. 2 K). Prevulvar setae numbering 3 pairs ( Fig. 2 L), each 86–137 µ m long. Antennae well developed, 8 segmented ( Fig. 2 M, Fig. 3 N), each 300–380 µ m long. Clypeolabral shield 125–140 µ m long, 129–160 µ m wide. Labium 52–69 µ m long, 85–110 µ m wide, with 4 setae 20–29 µ m long on each side. Legs well developed, each with a tibiotarsal sclerotization ( Fig. 2 N, Fig. 3 T) and free articulation; claw without denticle; tarsal digitules slender, knobbed, each 55–75 µ m long; claw digitules broad, equal, expanded at apex ( Fig. 2 O), each 38–47 µ m long. Hind trochanter + femur each 189–250 µ m. Anterior spiracles each 65–85 µ m long, 42–52 µ m wide across atrium. Posterior spiracles similar to anterior ones, each 62–88 µ m long, 49–58 µ m wide across atrium. Spiracles each without a sclerotic plate ( Fig. 2 P, Fig. 3 O). Spiracular pore bands each 1 or 2 pores wide, extending medially beyond apodemal base of spiracles. Spiracular pores quinquelocular ( Fig. 2 Q, Fig. 3 P), each 3–4 µ m in diameter, with 22–42 pores in each anterior spiracular pore band and 28–41 in each posterior band. Multilocular pores, each 5–7 µ m in diameter with 7 loculi ( Fig. 2 R, Fig. 3 Q), present in anal area, in transverse bands on each of posterior 4 abdominal segments, plus 2 to 3 on each of anterior abdominal segments and in a group of 3 or 4 laterad to each hind coxa ( Fig. 2 S). Tubular ducts of 3 types: Type I ( Fig. 2 T, Fig. 3 R1) with a well-developed terminal gland and short inner ductule; present medially on head and thorax; type II ( Fig. 2 U, Fig. 3 R2) a rather narrower duct with a much thinner inner ductule and a well-developed terminal gland present medially on posterior abdominal segments and in submarginal band, and type III ( Fig. 2 V, Fig. 3 R3) with a filamentous short inner ductule and very small terminal gland present in a band extending from anal cleft to posterior spiracular furrow. Microducts scattered ( Fig. 3 S), each 3–3.5 µ m long, 1–1.5 µ m wide.

Intraspecific variation and interspecific similarities. In slide mounts, P. urbicola resembles P.okitsuensis (Kuwana) and P. floccifera (Westwood) ( Qin & Gullan 1992; Tanaka & Amano 2006; Abdel-Razak et al. 2014). Qin and Gullan (1992) stated that the species lacks dermal areolations and submarginal tubercles completely in Australia, whereas Tanaka and Amano (2006) affirmed that both dermal areolations and dorsal tubercles are present but rare. Williams and Watson (1990) also stated that some P. urbicola possess submarginal tubercles. In the present study, all specimens had dermal areolations and dorsal tubercles were found in 2 out of 41 specimens. Dorsal dermal areolations was prominent but were present only in submarginal areas. Figure 1 shows variation in body colour at different developmental stages and in specimens developing on different host-plants. Hamon and Williams (1984) and Tanaka and Amano (2006) also provided colour photographs of the species in life.

Host plants and distribution. Although the surveys were conducted in 11 districts of Karnataka, P. urbicola was only collected in Bengaluru city. Out of the five host plants on which the scale was recorded, three were roadside plants, such as Pisonia grandis , Citharexylum spinosum and Lantana camera , in disturbed ecosystems, perhaps indicating that the crawlers were being dispersed by wind generated by passing vehicles. On all three hosts, the infestation was extremely heavy; the leaves had turned yellow and the trees/plants were eventually defoliated. Two further records were made on Solanum spp. growing inside polyhouses but the infestation levels were relatively low. As the polyhouses had controlled temperature and humidity, the chances of scale insect population explosion were very high; however, the pest was removed as soon as it was observed. All the hosts in the present study have been recorded previously elsewhere in the world. Pulvinaria urbicola is an extreme host plant generalist and is reported to attack species of dicots, monocots and ferns in 81 genera belonging to 33 plant families ( García Morales et al. 2015) Although it was not recorded on any economically important fruit crops in the present study, it could become a pest of some of the most important horticultural crops in India, such as Annona muricata L. ( Lincango et al. 2010), Citrus sp. ( Steinweden 1946), Litchi sinensis Sonn. and Psidium guajava L. ( Williams & Watson 1990), on which it has been recorded elsewhere. This insect can be easily transported and can spread passively through various means such as by mutualistic ants, external dispersal on birds and by wind currents ( Neumann et al. 2014).

Pulvinaria urbicola is widely distributed in tropical and subtropical countries, with distribution records from 51 countries on different continents ( García Morales et al. 2015).

Management. While discussing management practices for P. urbicola on Christmas Island, Neumann et al. (2014) stated that there are no feasible chemical options for direct control of this scale on a landscape scale; however, it has been controlled at least partially by the introduction of natural enemies ( Smith & Papacek 2001; Waterhouse & Sands 2001). Smith et al. (2004) reported successful biological control of this soft scale on Coringa South West Island (Queensland, Australia), where it became a destructive pest in Pisonia grandis forest. Cryptolaemus montrouzieri Mulsant ( Coleoptera : Coccinellidae ) has proved very effective in suppressing populations of P. urbicola on oceanic islands ( Neumann et al. 2014), while Panis and Maro (1977) described a method for mass-rearing the scale, although this publication was not available during the present study. However, we reared P. urbicola on summer squash ( Cucurbita pepo L.) for five generations ( Fig. 4A ). When adults and larvae of C. montrouzieri were released on the laboratory reared colony, they readily fed on the scale ovisacs and crawlers ( Fig. 4 B). Although no naturally occurring predatory coccinellids were collected in the present study, parasitoids such as Encyrtus aurantii (Geoffroy) and an indeterminate species of Metaphycus Mercet were recorded in small numbers. Sixteen specimens of E. aurantii and seven specimens of Metaphycus sp. were recovered from a colony of P. urbicola containing roughly 500 nymphs and adults, indicating low levels of parasitism in the field. These parasitoids, however, could be reared in the laboratory on scales reared on summer squash. The recent invasion by Paracoccus marginatus Williams & Granara de Willink and its successful management through classical biological control in India ( Shylesha et al. 2010), provides a good example for exploring possibilities of managing this pest by importing parasitoids from Jamaica and Equatorial Africa from where the pest is likely to have originated (García Morales, 2005).

Figures

FIGURE 1. Life stages of Pulvinaria urbicola Cockerell and colour variation in different stages and on different host plants A. Eggs and nymphs; B. Close-up of an adult female on Citharexylum spinosum; C. Nymphal stage on the branch of Solanum lycopersicum; D. Scale colony on Capsicum annuum; E. Adult females on the branch of Solanum melongena; F. Mature adult female on the stem of Pisonia grandis; G. Colony on a branch of Lantana camara; H. Laboratory reared colony on Cucurbita pepo; I. Colony of ovipositing females on under-surface of a leaf of Pisonia grandis.

FIGURE 2. Diagnostic characters of a slide-mounted adult female of Pulvinaria urbicola Cockerell.

FIGURE 3. Taxonomic illustration of an adult female of Pulvinaria urbicola Cockerell. A. Body derm; B. Marginal setae; C. Spiracular setae; D. Dermal areolation; E. Dorsal setae; F. Dorsal tubercle; G. Discoidal pores; H. Dorsal tubular duct; I. Dorsal microduct; J 1. Dorsal view of anal plate; J 2. Ventral view of anal plate; K. Anal ring; L. Submarginal setae, M. Ventral setae; N. Antenna; O. Spiracle; P. Spiracular pores; Q. Multilocular pore; R 1. Type I ventral tubular duct; R 2. Type II ventral tubular duct; R 3. Type III ventral tubular duct; S. Ventral microduct; T. Tarsus and claw.

FIGURE 4. A. A colony of Pulvinaria urbicola Cockerell reared on Cucurbita pepo fruit. B. Cryptolaemus montrouzieri Mulsant larva (indicated by the arrow) feeding on the ovisacs and crawlers of Pulvinaria urbicola.