A parasitic insect on a parasitic plant: a new species of the genus Formicoccus Takahashi (Hemiptera, Coccomorpha, Pseudococcidae) from Ishigaki Island, Japan

Abstract A new species of the genus Formicoccus Takahashi (Hemiptera, Coccomorpha, Pseudococcidae) collected from the holoparasitic plant Balanophorafungosa J. R. & G. Forst (Balanophoraceae), on Ishigaki Island, Japan, is described as Formicoccusyoshinoi Tanaka, sp. nov. based on the morphology of adult females. This species is similar to F.formicarius (1900) and F.erythrinae Williams, 2004, but differs from them by having fewer than six cerarii, and only one type of ventral oral collar tubular duct distributed on the medial area of the posterior abdominal segments. Keys to the Oriental species of the genus Formicoccus are provided.


Introduction
Mealybugs of the family Pseudococcidae (Hemiptera), are the second largest group of the infraorder Coccomorpha (García Morales et al. 2021). Adult females in this family are soft-bodied insects, commonly coated in white powdery wax with lateral wax filaments or have a waxy felted covering (Williams 2004). Members of the Coccomorpha, including mealybugs, are plant parasites, most of which suck sap from phloem tissue, and many are important crop pests (García Morales et al. 2021). Generally, mealybug species have been investigated from biological, agricultural, and economic perspectives.
To date, 78 species of mealybugs in 32 genera have been recorded in Japan (García Morales et al. 2021), many of which are important agricultural and horticultural pests (Kawai 1972(Kawai , 1980(Kawai , 2003 and have been relatively well-characterized taxonomically. However, there have been comparatively few taxonomic studies and faunal surveys of non-pest mealybug species, and it is believed that many species remain undescribed and unrecorded in Japan (Kawai 1980). In particular, faunal surveys of mealybugs that feed on certain minor and unique plant species groups, e.g., parasitic plants, ferns, grasses, and bamboos have not been well-studied in Japan, especially hypogeal species, thus many more mealybug species are likely to be present on these understudied host plants.
During a botanical survey led by the second author (KS) in the southwestern islands of Japan (the Ryukyu Islands), on Ishigaki Island, a unique undescribed species was found belonging to the genus Formicoccus (Pseudococcidae) parasitising a Japanese fungus root, Balanophora fungosa J. R. & G. Forst (Balanophoraceae), which is one of the non-photosynthetic and holoparasitic plants in Japan. The present study describes and illustrates the species as new to science based on the morphology of adult females. Keys to the Oriental species of Formicoccus are provided.

Materials and methods
The specimens described in the present study were collected on 14 December 2019 from Balanophora fungosa on Ishigaki Island, Japan, by Mr. Keiya Yoshino. The slidemounting method used followed the method described by Tanaka (2014). The morphology of the slide-mounted specimens was observed using a phase-contrast light microscope (BH2-PH; Olympus Corporation, Tokyo, Japan). The terminology and descriptive format used in the present study follow Williams (2004) and Tanaka and Kamitani (2021). The descriptions are based on multiple specimens, each character measurement is specified for the holotype, followed by the range of measurements for all type specimens in parentheses, if different. The type specimens of the species described below were deposited in the Ehime University Museum, Matsuyama, Japan (EUMJ) and the Entomological Laboratory, Faculty of Agriculture, Kyushu University, Fukuoka, Japan (ELKU). In the lists of material examined below, the collection data are listed as they appear on the slide labels, with "/" indicating the end of each line. Takahashi, 1928: 253 Type species. Formicoccus cinnamomi Takahashi, original designation.

Formicoccus
Key to adult females of Formicoccus species in the Oriental region (adapted and modified from Takahashi 1930Takahashi , 1940Tang 1992;Williams 2004)  Diagnosis. Slide-mounted adult female mostly oval. Anal lobes with well-developed and narrow anal lobe bar. Antenna mostly with seven segments and many flagellate setae. Legs relatively short and stout, but well developed. Hind legs with numerous translucent pores present on both dorsal and ventral surfaces of coxae. Circulus present between ventral abdominal segments III and IV. Ostioles present. Anal ring situated ca. half length from apex of abdomen or end of posterior abdominal segments, bearing 6 setae. Cerarii numbering fewer than 6 pairs; all cerarii situated on posterior abdominal segments. Dorsal setae slender, relatively long and flagellate, densely present and covering almost entire body surface. Dosal trilocular pores evenly distributed. Oral rim ducts and oral collar tubular ducts absent on dorsum. Discoidal pores sparsely distributed on both body surface. Multilocular disc pores mostly present in medial area of ventral abdominal segments VI-IX. One size of oral collar tubular ducts present on venter, forming an irregular submarginal band on posterior abdominal segments and forming transverse rows on medial area of abdominal segments VI-IX.
Description (n = 7). Live adult female feeding on the underground part of host plant (Figs 1, 2) and secreting white powdery wax on all body surfaces (Figs 1, 2). Body shape of mature adult female mostly hemispherical in shape (Fig. 2).
Venter. Ventral derm with slender flagellate setae, each 31-123 (15-123) µm long, longest on medial area of posterior abdominal segments. Multilocular disc pores, each 7-9 (6-9) µm wide, mostly present in medial area of abdominal segments VI-IX. Trilocular pores ca. 3-4 µm wide, evenly distributed. Oral rim ducts absent. Oral collar tubular ducts present, of one size, each with outer ductule 2-4 µm in diameter (slightly smaller than that of a trilocular pore) forming an irregular submarginal band on posterior abdominal segments and forming transverse rows on medial area of abdominal segments VI-IX. Discoidal pores slightly smaller than trilocular pores, sparsely present on body surface.
Host plants. Balanophora fungosa (Balanophoraceae). Biology. Balanophora fungosa is characterized by unusual mushroom-shaped inflorescences that emerge above the ground and warty tubers that are attached to their host plants (Hansen 1972). Specimens of Formicoccus yoshinoi were found in aggregations on the tuber of this species. Given that (i) no other plants associated with F. yoshinoi Tanaka, sp. nov. were found during the survey and (ii) B. fungosa individuals infected by F. yoshinoi Tanaka, sp. nov. were found at two independent sites, this species might be a specialist on Balanophora species. It is worth investigating whether the species feeds on other plant species.
Remarks. In his taxonomic revision of the genus Formicoccus Takahashi, 1928, in Southern Asia, Williams (2004 emphasised the following morphological character states as defining morphological features of the genus: the presence of 18 pairs of cerarii, the presence of anal lobe bars on the ventral side of the anal lobe, and the presence of more than two cerarian setae on at least some abdominal cerarii. However, there are exceptions in the first two-character states, with a species with fewer than 17 pairs of cerarii (F. tripurensis) and a species with an uncertain presence of anal lobe bars (F. lingnani) were included in the genus. The species described in this study also does not have 18 pairs of cerarii, and the species' anal lobe bars are quite fainted and often difficult to see in a few specimens. Danzig and Gavrilov-Zimin (2015) rejected the use of anal lobe bar as a generic character state of the genus Formicoccus. They regarded that the presence or absence of the anal lobe bar fell into individual variations and instead used the presence of more than six setae in the anal ring as a critical generic character state of the genus. According to their opinion, the species described in this study are not Formicoccus. However, the debate on the definition of the genus Formicoccus is still ongoing, and no consensus has been reached yet. Zhang and Wu (2017) regarded the number of anal ring setae as having no generic significance. Based on their studies, the anal ring typically bears six basic setae, and when more setae are present, the extra setae are usually slender and short, and vary in their positions. They placed some species with anal lobe bars (F. citricola and F. sinensis (Borchsenius, 1962)) in the genus Formicoccus. It is clear that a more detailed study is required to better understand the importance of such morphological character states, particularly using a combination of molecular and morphological characters. Under these circumstances, we tentatively included the species described in this study into the genus Formicoccus.
Formicoccus yoshinoi Tanaka, sp. nov. is similar to F. formicarius (Newstead, 1900) in having: (i) long flagellate dorsal setae; (ii) relatively short and stout legs; (iii) only one type of ventral oral collar tubular duct; and (iv) a round body shape, but differs from this species as follows (characters of F. formicarius are given in parentheses): (i) having fewer than six cerarii with 0-6 conical cerarian setae (with 18 pairs of cerarii with long and stout flagellate setae); and (ii) having a transverse row of ventral oral collar tubular ducts on the medial area of posterior abdominal segments (lacking ventral oral collar tubular ducts on medial area of abdominal segments). The species is also similar to F. erythrinae Williams, 2004, in having: (i) long flagellate dorsal setae; (ii) relatively short legs; and (iii) round body shape, but differs from the latter species as follows (characters of F. erythrinae are given in parentheses): (i) having fewer than six cerarii (having 18 cerarii); and (ii) having only one type of ventral oral collar tubular duct (with two types of ventral oral collar tubular ducts).
Etymology. Named after the collector of type series, an independent researcher of plants in Ishigaki Is., Mr. Keiya Yoshino.