Redescription of Takahashia citricola Kuwana, 1909, and its transfer to the genus Pulvinaria Targioni Tozzetti (Coccoidea, Coccidae)

Abstract The Japanese soft scaleTakahashia citricola Kuwana, 1909 is redescribed and transferred to the genus PulvinariaTargioni Tozzettias Pulvinaria citricola (Kuwana, 1909), comb. n.(Coccoidea: Coccidae). Pulvinaria gamazumii Kanda, 1960 is synonymized with Pulvinaria citricola comb. n. and Pulvinaria nipponica Lindinger, 1933, is resurrected as the replacement name for Pulvinaria citricola Kuwana, 1914 (nec Kuwana, 1909). The adult female of Pulvinaria citricola (Kuwana, 1909) is redescribed and illustrated.


Introduction
Soft scale insects belong to the family Coccidae which is of the third largest family in the superfamily Coccoidea (Hemiptera: Sternorrhyncha), with more than 1100 species described until now (Ben-Dov 2012a). Like members of other families of the Coccoidea, species in the family Coccidae are known for their peculiar morphology compared with other "normal" insects, and are also economically important as plant pests. Like aphids (superfamily Aphidoidea), they suck plant sap and host plants affected by them will become debilitated or die if their populations become too high. Their "honeydew" can cause sooty molds on plant surfaces and cause indirect damage to the plant by reducing their photosynthetic activity. Furthermore, some soft scale insects are known as vectors of serious plant diseases such as Grapevine leafroll (Belli et al. 1994, Fortusini et al. 1997, Hommay et al. 2008. Thus, control of soft scale insects and the study of their taxonomy are very important issues for worldwide crop production, especially for fruit crops. In Japan, 72 species of soft scales (Coccidae) in 21 genera have been recorded (Ben-Dov 2012b, 2012c), but Japanese genera and species of Coccidae are still in need of study. An example is the Japanese species Takahashia citricola Kuwana, 1909, for which the adult female has a discal seta on each anal plate -a feature considered diagnostic for members of the genus Saissetia Déplanche. Probably for this reason, T. citricola has been treated as S. citricola (Kuwana 1909) (Takahashi andTachikawa 1956, Ben-Dov 1993). However detailed study of the morphology of T. citricola (presented below) shows that it should be transferred to the genus Pulvinaria Targioni Tozzetti. However the name 'citricola' is in use in Pulvinaria for a different species, P. citricola Kuwana, 1914(nec Kuwana, 1909, which thus becomes a junior homonym. Pulvinaria nipponica Lindinger, 1933, is resurrected here as the replacement name for P. citricola Kuwana, 1914. The adult female of P. citricola (Kuwana, 1909) is redescribed and illustrated and some taxonomic features of the species are discussed.

Materials and methods
The scale insect samples studied were collected by several Japanese coccidologists (S. Kanda, S. Kawai and R. Takahashi) plus newly collected specimens. The slide-mounting method for the newly collected specimens followed that of Kawai (1980). The morphology of the slide-mounted specimens was examined under a phase-contrast light microscope (Olympus BH-2 PH). Terminology follows Hodgson (1997). Specimens examined in this study are deposited in the Osaka Museum of Natural History, Osaka (OMNH), The Laboratory of Systematic Entomology, Faculty of Agriculture, Hokkaido University, Sapporo (SEHU), and at the Kawai scale insect collection deposited at Tokyo University of Agriculture, Tokyo (TUA).
Description. Living appearance. Body nearly round, broadest across thorax and anterior abdomen. Prior to oviposition, dorsum reddish light brown posteriorly and dark brown anteriorly (Fig. 1), changing to reddish brown with a dark brown marginal ring at full-maturity. Mature adult females produce an ovisac mainly from beneath abdomen. No wax present on dorsum at oviposition. Post-oviposition females sclerotised and not shrivelled. Ovisac white, very convex, nearly hemispherical. Body strongly lifted posteriorly by ovisac.
3.5-7.0 mm wide, consisting of a compact group of 2-11 pores anterior to anal plates. Dorsal tubular ducts absent. Dorsal microductules frequent throughout. Dorsal tubercles absent. Anal plates posteriorly elongated; each plate with posterior margin about two times as long as anterior margin, each with 3 fine apical setae and a discal seta; length of plates 214-249 mm; width of single plate 85-122 mm; each plate with well-developed supporting bars. Ano-genital fold with 2 pairs of setae along anterior margin and 1 or 2 pairs laterally. Anal ring with 6-8 setae (mostly 8).

Eyespot present near margin
Margin. Marginal setae spinose, each with a simple pointed apex and a well-developed basal socket; length highly variable, each seta 20-107 mm long, with 10-13 setae present on each side between stigmatic clefts. Stigmatic clefts shallow, each with 0-3 (mostly 3) stigmatic spines in each cleft, longest spine 92-134 µm long, about 3-4 times as long as lateral spines. Venter. Derm membranous. Pregenital disc-pores each with 8-11 loculi (mainly 10), present around genital opening and on mediolateral areas of all abdominal segments and metathorax; a small group also present laterad of each coxa. Spiracular disc-pores each with 5 loculi, present between margin and each spiracle in band 1-5 pores wide; anterior bands with 30-63 pores and posterior bands with 45-80 pores. Ventral microducts evenly distributed throughout venter. Three types of ventral tubular ducts present: type I with well-developed terminal gland and a stout inner ductule, present medially on head and thorax; type II rather narrower with a long, much thinner inner ductule, shallow cup-shaped invagination, and a well-developed terminal gland, sparse medially on posterior abdominal segments and also in a submarginal band with ducts of type III; type III ducts similar to type II, but with a short, filamentous inner ductule and very small terminal gland, mainly present in a broad submarginal band. Ventral setae: 3 pairs of long pregenital setae and 3-6 pairs of long setae between antennae; other setae short and fine. Spiracles as usual for family; width of each peritreme: anterior 47-60 mm, posterior 58-70 mm. Legs well developed; each with tibio-tarsal articulation and articulatory sclerosis; all claws without denticle; both claw digitules rather broad and slightly shorter than thin tarsal digitules; trochanter + femur 240-306 mm, tibia 162-198 mm, and tarsus 92-118 mm. Antennae each with 7 or 8 segments (mostly 8); total length 342-412 mm. Labium approximately 47-118 mm wide.

Discussion
Pulvinaria citricola comb. nov. resembles the Japanese species P. nipponica stat. res., P. kuwacola Kuwana and P. photiniae Kuwana in the distribution of type III ventral tubular ducts and the shape of marginal setae. However, it is easily distinguishable from those three species in having a well-developed discal seta on each anal plate and by the shape of the anal plates which are posteriorly elongated (P. nipponica, P. kuwacola and P. photiniae lack discal setae and their anal plates are together quadrate and not elongated posteriorly).
Most soft scales in the genus Saissetia (Coccidae: Coccinae: Saissetini) also have a discal setae on the anal plates and this is considered a diagnostic feature of the genus Watson 1990, Hodgson 1994). Takahashi and Tachikawa (1956) probably considered this feature when they transferred Takahashia citricola to the genus Saissetia, though they did not clearly express the reasons for the transfer. However, the distributional pattern of the ventral tubular ducts of P. citricola (Kuwana, 1909) greatly differs from most species of Saissetia including the type species of the genus and is similar to that of many Pulvinaria species. Furthermore, ovipositing adult females of P. citricola (Kuwana, 1909) produce a well-developed ovisac (see Kawai 1980), which is the most important diagnostic feature of the genus Pulvinaria and all of the related genera in the tribe Pulvinariini.