A new African soft scale genus, Pseudocribrolecanium gen. nov. (Hemiptera: Coccoidea: Coccidae), erected for two species, including the citrus pest P. andersoni (Newstead) comb. nov

A new African genus of soft scale insects, Pseudocribrolecanium gen. nov. is erected to accommodate Akermes colae Green & Laing and Cribrolecanium andersoni (Newstead). The adult females and first-instar nymphs of the two species are redescribed and illustrated. Taxonomic keys to separate the adult females and first-instar nymphs are provided. The affinity of Pseudocribrolecanium with the tribe Paralecaniini in the subfamily Coccinae is discussed.


Introduction
There are about 270 species in 56 genera of soft scale insects (Hemiptera: Coccoidea: Coccidae) hitherto described from the African continent (Ben-Dov et al. 2005). These have been described mainly during two periods: (i) from 1899-1941, during which more than one hundred species were named by such early workers as Newstead, Hall, Green, andLaing, and(ii) from 1954-1979 when about another hundred species were added mainly by De Lotto and Hodgson (Ben-Dov et al. 2005). Since then, various authors, including Hodgson, have sporadically contributed to the knowledge of the coccid fauna of Africa. Despite its rich flora, which includes 6 biodiversity hotspots (Myers et al. 2000;Myers 2001), the number of described coccid species recorded in the African continent has not increased in the last 10 years, undoubtedly because of the lack of taxonomic specialists in the region.
The author had the opportunity to travel to Ghana in June, 2005, and collected scale insects of various families including the Coccidae, Diaspididae, Margarodidae, Ortheziidae, Pseudococcidae and Stictococcidae. Among the coccids, a scale insect later identified as Akermes colae was collected on the leaf of a cacao tree. The genus Akermes Cockerell (1902) currently includes 14 species distributed in Central and South America (10 species), India (1 species), Australia (2 species), and Africa (1 species). The author has studied the genus Akermes previously and considers that it is endemic to the New World (Kondo & Williams 2004). Attempts were therefore made to allocate A. colae to an appropriate genus. When Green & Laing (1924) described Akermes colae, they pointed out that A. colae was structurally very similar to A. andersoni (referred to as Lecanium andersoni). De Lotto (1968) redescribed A. bruneri Cockerell, the type species of Akermes, and stated that A. andersoni had little in common with the genus Akermes and transferred it to Cribrolecanium Green (1921). However, De Lotto (1968) did not study A. colae, and it has remained in the genus Akermes until the present.
Cribrolecanium currently contains 3 species, 2 from the Oriental region and C. andersoni from the Afrotropical region (Ben-Dov et al. 2005) although the latter species has been considered only doubtfully congeneric (Hodgson 1994) based on adult female morphology. However, studies based on crawler morphology suggest that C. andersoni is definitely not congeneric Williams and Kondo 2002). As indicated by Green & Laing (1924), C. andersoni and A. colae are closely related, but do not fit into any known genus, and thus a new genus Pseudocribrolecanium is erected here to accommodate them.

Materials and Methods
Specimens were slide mounted according to methods discussed by Kosztarab (1996) and Kondo & Gullan (2005). Morphological terminology follows mostly that of Hodgson (1994). Measurements of specimens were made using an ocular micrometer on an Olympus phase-contrast microscope. The illustrations of the coccids follow the style adopted for the Coccoidea, with the dorsal surface drawn on the left side of the drawing and the ventral surface drawn on the right, with enlargements of important features placed around the illustration. The total number of specimens used for each description is given in parentheses, e.g. (n=48). In the material studied, the number of slides and specimens on each slide are given as the number of slides followed by the total number of specimens and their corresponding stages; for example, 1 slide with 1 second-instar female and 1 adult male specimen would be: 1(2: 1 second-instar female + 1 adult male). The stage is not given if all specimens are adult females.

Generic diagnosis, adult female
Insects oval, pyriform to asymmetrical in shape, flat, becoming sclerotized at maturity.

Dorsum.
Derm membranous, becoming highly sclerotized at maturity. Dorsal setae short, sharply spinose. Simple pores present or absent. Dorsal microducts present, rather few, scattered throughout dorsum. Translucent furrows present, associated with stigmatic areas and often elsewhere; furrows either touching or not touching margin. Dorsum usually with several cribriform plates, although occasionally absent on P. colae. Dorsal tubercles and tubular ducts absent. Preopercular pores usually present in a longitudinal line anterior to anal plates. Anal plates together quadrate or inverted pyriform, dorsal surface with 3 or 4 apical or subapical setae, plus 1 seta on inner margin of each plate. Anal ring with 4 pairs of setae and an irregular row of translucent wax pores. Eyes present, represented by clear areas located on dorsal submargin.

Margin.
Derm heavily sclerotized in a narrow band around margins. Marginal setae numerous, slender, flagellate, arranged in a single row. Stigmatic clefts shallow or absent, with 3, rarely with fewer or up to 5 stigmatic setae; with either one seta longer than others or all subequal in length.
Antennae each 2-5 segmented, segmentation indistinct; fleshy setae present only on last antennal segment and setae often knobbed. Legs greatly reduced, segmentation poorly defined; claws without a denticle. Spiracles rather small.
Dorsum. Dorsal derm membranous. Dorsal setae short, present in 2 longitudinal parallel rows of 5 setae. A trilocular pore present on each side of head region near margin. Dorsal microducts present in a submarginal and 2 submedian longitudinal rows, with a few additional microducts on thorax between the submedian and submarginal rows. Simple pores each closely associated with a microduct. Anal plates each triangular, dorsal surface with a shingled texture and 3 apical setae, 1 seta along inner margin of each plate, with 1 fringe seta and 1 ventral subapical seta. Anal ring with 3 pairs of setae and an irregular row of translucent wax pores. Eyes located on margin on area laterad to each antennal scape.
Margin. Outline smooth. Marginal setae slender, total 34, with 8 anteriorly between eyes and, on each side, 3 between each eye and anterior stigmatic setae, 2 between each anterior and posterior stigmatic setae and 8 between each posterior stigmatic setae and posterior end. Stigmatic setae in groups of 3, well differentiated from marginal setae; median seta bluntly spinose, or clavate; lateral setae short, bulbous, length about 1/5-1/11 of median seta.
Venter. Ventral derm membranous. Pairs of submedian abdominal setae present on last 3 abdominal segments. Submarginal setae arranged in a parallel row of 7 on each side of abdomen, plus 1 submarginal seta between each anterior and posterior spiracle, and 1 submarginal pair of setae near apex of head. Interantennal setae 1 pair. With 1 ventral microduct present between each pair of submarginal setae on abdomen and 1 between each anterior and posterior spiracle. Spiracular disc-pores each with 3 loculi; 3 or 4 pores between each anterior and posterior spiracle and margin. Mouthparts normal; labium with 4 pairs of labial setae. Legs well-developed; microctenidia present on tibial apex. Prothoracic tarsal digitules dissimilar, one knobbed and other spiniform; mesothoracic and metathoracic tarsal digitules similar, both knobbed. Spiracles normal, with a well developed muscle plate. Claws each with a denticle; claw digitules knobbed, one slightly broader than other. Antennae each 6-segmented, with 3rd antennal segment longest; fleshy setae present on last 3 apical segments; 1 single fleshy seta on segment 4, 1 fleshy seta plus 1 setose seta on segment 5, and several fleshy and setose setae on terminal segment.

Etymology
The genus name is derived from the prefix Pseudo-(Greek), meaning something superficially 1. Dorsum with both large and small cribriform plates, smaller plates near margin each 10-80 µm wide, larger plates farthest from margin each 100-180 µm wide; present in about 2 or 3 irregular rows totaling 12-22 around body P. andersoni (Newstead), comb. nov.

Description
Adult female (Fig. 1) Unmounted material. Insects completely covered with rather dense, dusky-white, mealy secretion. Color on removal of secretion, rich dark piceous or very dark castaneous, shining; younger specimens varying from reddish brown to dusky buff. Form irregularly oval, asymmetrical, more or less narrowed in front; sometimes broadly ovate or subcircular. Flat or very low convex, with faint median keel in abdominal region; sides well within margin. Derm densely sclerotized, especially towards margins; with innumerable minute, translucent poreless cells (Newstead 1917).

Dorsum.
Derm often with areolations, particularly expressed submarginally (Fig. 1B). Dorsal setae (Fig. 1E) sharply spinose or conical, each 5-9 µm long. Simple pores (Fig. 1G) about 1.8 µm wide, scattered on dorsum. Dorsal microducts (Fig. 1F) each about 1.8 µm wide, scattered on dorsum. Translucent stigmatic furrows present as in diagnosis, usually with an additional translucent lateral furrow on head and two on abdominal region. Cribriform plates (Fig. 1A) oval to elongate oval, occurring either submarginally or submarginally and submedially, totaling 12-22; varying in size, plates closer to margin smallest, each about 10-80 µm wide, innermost plates largest, each 100-180 µm wide. Preopercular pores present in a linear group of about 10-40 pores anterior to anal plates, often displaced anteriorly onto the thoracic and head region with pores completely absent just anterior to anal plates (as reported by Almeida 1969), or form a long line of pores extending from area just anterior to anal plates up to head region. A sclerotic area often present around anal plates. Anal plates (Fig. 1H) together inverted pyriform or quadrate, with round angles, located at about 1/6 of body length from posterior margin, each plate 117-121 µm long, 53-58 µm wide; anterolateral margin 62-70 µm long, posterolateral margin 98-107 µm long, with 3 or 4 setae on dorsal surface, plus 2 pairs of fringe setae and about 2 ventral subapical setae. Anal ring (Fig. 1J) as in diagnosis. Eyes present, represented by clear subcircular areas located on dorsal submargin (see arrow on Fig. 1).

Morphological variation.
Two specimens from Kenya labeled as A. andersoni collected on Ficus sp. are strongly asymmetrical and resemble P. colae. Their largest cribriform plates are rather small, each 40-80 µm wide, smallest cribriform plates each 10-40 µm wide. The cribriform plates in these species are arranged mostly in a single marginal row although there are places with definitely an inner and outer row as in the rest of the material of P. andersoni. The total number of cribriform plates in the Kenyan specimens are 14 and 16 respectively and fall also in the range of P. andersoni. Whether the specimens collected on Ficus sp. should belong in a different species needs further study. Measurements of the above specimens were excluded from the description.

Biology (from Brink 1998)
The white powdery scale is a polyphagous insect known as a pest of citrus. The adult female is completely covered with a dense white powdery secretion, which also spreads over the surrounding parts of the host plant giving infested leaves an almost uniform white powdery appearance. P. andersoni feeds on leaves and young shoots, but does not feed on the fruit and branches. The honeydew serves as a substrate for the saprophytic sooty mold fungi of the genus Capnodium. In South Africa, the insect is found throughout the year, where it appears to have three field generations per year. Various natural enemies of P. andersoni are known, including the hymenopterous parasitoids Coccophagus philippiae (Silvestri), C. pulvinariae Compere, C. lycimnia (Walker), Coccophagus sp.

Diagnostic features
The adult female of P. andersoni (Newstead) can be easily separated from P. colae by the following combination of characters: (i) presence of both large and small cribriform plates on P. andersoni (all small on P. colae ), (ii) difference in number of cribriform plates, with 10-22 in P. andersoni, but only 0-9 on P. colae, (iii) body shape, which is oval to only slightly asymmetrical in P. andersoni but highly asymmetrical in P. colae, and (iv) the presence of obvious simple pores (not detected on P. colae ). Furthermore, the first-instar nymphs of P. andersoni have (v) bluntly spinose stigmatic seta whilst they are clavate on P. colae, and (vi) the head has a round contour whereas it is tapering in P. colae.
Paralectotypes. GHANA, same data as lectotype, mixed slide, 1(6: 1 hymenopteran larva + 4 adult Parasaissetia nigra (Nietner) + 1 adult P. colae ): paralectotype conspecific with lectotype clearly indicated on label: longest of all specimens on slide ca. 3.5 mm (at greatest length) (BMNH). Note. The collection data of the lectotype and paralectotype herein designated matches well the data given in the original description by Green & Laing (1924). However, the paralectotype slide is composed of a mixture of specimens of which only one specimen is conspecific with the lectotype. The remaining specimens include four adult females of the coccid Parasaissetia nigra (Nietner) and one hymenopteran larva (probably a parasitoid). It is common to find one or two, and even more species together on one host plant. The mixing of species on this one slide probably occurred because the adult females of the two coccid species resemble each other superficially in life, e.g., P. nigra and P. colae both become heavily sclerotized at maturity and their body shape is somewhat similar being pointed at both extremities.
Morphology not recorded.

Margin.
Margins becoming heavily sclerotized in a narrow band around entire body on older specimens. Marginal setae (Figs 3C, 4C) flagellate, each 62-72 µm long, arranged in a single row, numerous, with 23-31 on each side between anterior and posterior stigmatic areas. Stigmatic clefts very shallow or absent; each with 3, rarely 4  stigmatic setae (Figs 3B, 4A&B), often absent or broken off in some stigmatic areas; each setae sharply spinose, rarely bifurcate, 7.5-20 µm long; median seta longest, or all subequal in length.

Morphological variation.
A specimen recently collected in Ghana (Fig. 4) has fewer translucent furrows, no lighter patches around submargins and no cribriform plates. The degree of sclerotization appears to be highly variable in P. colae. Thus the main difference between the specimen from Ghana and those from the type series is the presence or absence of cribriform plates. More material is needed to determine if the specimen without cribriform plates is part of the morphological variation of A. colae or a separate closely-related species.

Unmounted material.
Morphology not recorded.

Biology
No information on the biology of P. colae has been published. The single specimen of the form without cribriform plates collected recently in Ghana was on the under surface of a leaf of Theobroma cacao alongside the leaf vein. The presence of second-instar males (see Material studied) suggests that the species reproduces sexually.

Diagnostic features
See diagnostic features under P. andersoni.

Discussion
Pseudocribrolecanium appears similar to Cribrolecanium Green (Myzolecaniinae), with which it shares dorsal cribriform plates and highly reduced appendages. However, this resemblance is superficial. Cribriform plates are also present on some other coccids. Hodgson (1994)  Cribrolecanium possesses the following features that separate it from Pseudocribrolecanium (character states on Pseudocribrolecanium in brackets): (i) the presence of a membranous bag-like structure which contains the spiracular pores (see Hodgson 1995) (spiracular disc-pores not within a bag-like structure), (ii) the restriction of pregenital disc-pores to immediately around the vulvar region (spreading anteriorly), (iii) the lack of spiracular setae (3-5), (iv) complete absence of preopercular pores (present), (v) presence of small groups of dorsal microducts on area anterior to anal plates (absent), (vi) antennal length less than the width or only slightly longer, never twice its width (length of antennae 3-4 times its width), and (vii) an anal ring with 16-18 setae (8 in Pseudocribrolecanium ). The two genera also differ greatly at the ecological level, with Cribrolecanium being found on the roots and in hollow branches of its host, whereas Pseudocribrolecanium feeds on the leaves.
Pseudocribrolecanium shares important features with the Paralecaniini (Coccinae), particularly with species of the genus Paralecanium Cockerell. These shared features are: (i) the position of the eyes on the dorsum away from the margin, (ii) a marginal sclerotized band, (iii) translucent furrows, and (iv) numerous marginal setae. However, in Paralecanium, as well as other genera in the Paralecaniini, the multilocular disc-pores are restricted to immediately anterior to the genital opening and the stigmatic clefts are usually quite distinct (Hodgson 1994). In Pseudocribrolecanium, the multilocular disc-pores are found also on some anterior abdominal segments, and the stigmatic cleft is poorly developed or lacking. In addition, the morphology of the first-instar nymphs does not support a close relation with the Paralecaniini. Very few studies have described or illustrated the first-instar nymphs of the Paralecaniini, but those species which have been described (e.g., Austrolecanium cappari (Froggatt), A. sassafras Gullan & Hodgson, Maacoccus cinnamomicolus (Takahashi), Paralecanium paradeniyense Green, P. planum (Green), and Xenolecanium takahashii Kondo) share many important features, i.e., a seta next to each mesothoracic and metathoracic coxa, six pairs of ventral submedian setae, and stigmatic setae positioned submarginally on either side of a deep stigmatic cleft (Gullan & Hodgson 1998, Hodgson and Martin 2001, Kondo et al. 2005. However, on the first-instar nymphs of Pseudocribrolecanium, the stigmatic clefts are very shallow, the stigmatic setae are positioned along the margins and not on the sides of a deep stigmatic cleft, and no seta is found next to either the mesoand metathoracic coxae, suggesting that Pseudocribrolecanium is not closely related to the Paralecaniini despite the similarities shared by the adult females. Further studies using additional material, molecular techniques and adult males, may help elucidate the phylogenetic position of Pseudocribrolecanium.