A new genus and species of Rhizoecidae (Hemiptera, Sternorryncha, Coccomorpha) associated with Acropyga yaeyamensis (Hymenoptera, Formicidae, Formicinae)

Abstract Ishigakicoccus gen. n. shimadai sp. n. is described based on the adult female morphology. This new species was found in the nest of a rare Japanese ant, Acropyga yaeyamensis Terayama & Hashimoto, 1996, in Ishigaki Is., Japan. It resembles Capitisetella migrans (Green, 1933) and Pseudorhizoecus proximus Green, 1933. However, the new species differs from those two species in having small multilocular pores, large 3-5 locular pores on the medial area of ventral abdomen, and two different-sized body setae. This new species is also the first record of a potential trophobiont of Acropyga yaeyamensis. A key to Japanese species of Rhizoecidae is also provided.


Introduction
Rhizoecidae is a family of Coccomorpha (Hemiptera: Sternorryncha) which members mostly live underground, feeding on plant rootlets (Williams 1998), and are known as "root mealybugs" or "ground mealybugs". The family is composed of 240 nominal species distributed in 18 genera (García et al. 2016), and 11 species distributed in five genera have been recorded from Japan (Tanaka 2016). Some species of the family are regarded as potentially or actually important plant pests (Danzig et al. 2008;Hambleton 1976;Kawai 2003;Williams 1996), and they are investigated from biological in addition to agricultural and/or economic perspectives.
Some genera and species placed in Rhizoecidae, especially those classified in the tribe Xenococcini, show very close trophobiotic relationships with ants that belong to the genus Acropyga (Hymenoptera: Formicidae: Formicinae) (Kishimoto-Yamada et al. 2005;LaPolla et al. 2002;LaPolla et al. 2008). Trophobiosis is commonly observed in interactions among many ants and honeydew-producing insects, including some scale insects, but the relationship between Acropyga ants and their trophobiont Rhizoecidae species is known as one of the most peculiar examples. Virgin queens of Acropyga ants grasping and carrying a root mealybug by their mandibles emerge from their nests for their mating flight and subsequent colony founding (LaPolla et al. 2002;LaPolla et al. 2008), the mealybugs are maintained in the ant's nest (Flanders 1957;Kishimoto-Yamada et al. 2005;LaPolla et al. 2002), and the ants feed on the honeydew excreted by the mealybugs, which in turn feed on root-sap (Johnson et al. 2001;Smith et al. 2007). This obligatory relationship has greatly interested many researchers, and as a result mealybugs and other scale insects associated with Acropyga ants have been relatively well studied systematically and/or taxonomically (LaPolla et al. 2008;Maruyama et al. 2013;Schneider and LaPolla 2011;Williams 1998;Williams 2004;Williams and LaPolla 2004;Williams and Terayama 2000). Nevertheless, a mutualistic partner or associate of a rare Japanese ant species, A. yaeyamensis, have not been hitherto detected nor described.
Recently, the author had an opportunity to examine several interesting mealybug specimens that were collected from the nest of A. yaeyamensis which showed a close association with the ant (Figure 2), being a potential mutualistic trophobiont. The species is quite peculiar and distinctive among known Rhizoecidae species, although it is somewhat similar to Capitisetella migrans and Pseudorhizoecus proximus.
This paper describes and illustrates this mealybug as a new genus and species on the basis of adult female morphology. A key to Japanese species of Rhizoecidae is also given.

Materials and methods
Specimens of the root mealybug species used in this study were originally collected by a collaborator of this study, Mr. Taku Shimada, on 16 February 2015, from a nest of A. yaeyamensis Terayama & Hashimoto, 1996, in Mt. Omoto, Ishigaki Is., Japan. The mounting method used for these specimens followed that described by Tanaka (2014). Morphology of the slide-mounted specimens was examined under a phase-contrast light microscope (Olympus BH2-PH). The terminology used to describe the adult females followed that of Kozár and Konczné Benedicty (2007). All examined type materials in this study are deposited in the National Museum of Nature and Science, Tsukuba, Japan (NSMT).

Subtribe Ripersiellina Kozár, 2007
Type genus. Ripersiella Tinsley, 1899 in Cockerell 1899 Diagnosis. Same as the family, except the characters related to Xenococcini, Geococcina and Rhizoecina. Most of the species have bitubular pores, and 5-6 segmented antennae. In some monotypic genera, included tentatively, the anal ring and/or the antennae are reduced (adopted and modified from Kozár and Konczné Benedicty 2007).
Diagnosis. Body elongate oval, slightly pyriform. Eye spot absent. Antennae 5 segmented. Legs well-developed. Two types of body setae present on both dorsal and ventral body surface. Small sized multilocular pores present, each with 5-6 loculi. Tritubular and bitubular pores absent. Oral collar tubular ducts absent. Ostioles absent. Anal ring irregular oval; anal pores and anal ring setae absent. Large 3-5 locular pore without central hub, present on medial area of ventral abdomen. A circulus present.
Etymology. Named after the island (Ishigaki) where the type species was collected first. The suffix coccus is commonly used in naming Coccomorpha genera. Gender: masculine.
Dorsum: Two types of body setae present. Type I: relatively well developed setae, 19.7-58.9 µm long, some setae with a bent or rarely with a knobbed apex. Type II: relatively slender setose setae, 11.0-32.8 µm long, each with a pointed apex. Both types of setae distributed in transverse segmental rows. Multilocular pores each about 2.9-3.7 µm in diameter, each with 5-6 loculi, present on head and thorax, but rarely present on abdomen (Figure 3). Tritubular and bitubular pores absent. Oral collar tubular ducts absent. Ostioles absent. Anal opening 38.9-52.6 µm long and 55.2-61.8 µm wide. Anal ring irregular oval. Anal pores, and anal ring setae absent, but type I and II setae densely present around the opening.
Etymology. Named after the collector of the type specimens. Host plant. Unknown.

Discussion
The genus and species described in this paper slightly resembles two other species of the monotypic genera of Rhizoecidae, Capitisetella migrans (Green, 1933) and Pseudorhizoecus proximus Green, 1933, in lacking ostioles and tritubular and/or bitubular pores, and having a pyriform to round body shape. However, the former is clearly distinguishable from those two species by having small multilocular pores on both surfaces of the body, 3-5 large locular pores on the medial area of the ventral abdomen, and two different-sized body setae. These morphological differences are here considered as good for the establishment of a new genus. Based on some morphological similarity, the genus and species is tentatively placed in the subtribe Ripersiellina Kozár 2007 of the tribe Rhizoecini Williams, 1969, in which C. migrans and P. proximus are also placed (Kozár and Konczné Benedicty 2007).
In east and southeast Asia, many species in tribe Xenococcini have been frequently found in Acropyga ants' nests (Williams 1998), and the xenococcine species appear to be the main mutualistic partners of Acropyga ants. However, the new species described in this paper is clearly different from all of them in having small multilocular pores, 3-5 locular pores, and 5 segmented antennae. Although the exact phylogenetic position of this new species is still unclear, but morphological features of the specimens indicate that this species apparently does not belong to tribe Xenococcini.
The collector of the species, Mr. Taku Shimada, observed some A. yaeyamensis workers grabbing and carrying the root mealybug individuals by their mandibles when he collected the species (Figure 2). This behavioral observation, the collecting site of the species, i.e. inside a nest of A. yaeyamensis and the morphological features of the species, i.e. the lack of wax on the body surface (Figure 1 and Figure  2), which is usually observed in most myrmecophilous scale insects (LaPolla et al. 2008) indicates that the species is a potential trophobiont of A. yaeyamensis, even though it does not appear to be a xenoccocine species. Similar associations between Acropyga ants and scale insects that are not members of the tribe Xenococcini have been sometimes, but not commonly, observed in the neotropics, the United States, and Australia (LaPolla et al. 2002;LaPolla et al. 2008;Jonson et al. 2001;Williams 1998;Williams and LaPolla 2004). One of the most extraordinary cases was observed in Australia; an ortheziid scale insect, Acropygorthezia williamsi LaPolla & Miller, 2008, which belongs to the family Ortheziidae, not Rhizoecidae, showed a close trophobiotic association with Acropyga myops (LaPolla et al. 2008). Intensive molecular phylogenetic analysis of scale insects having trophobiotic associations with Acropyga ants, including non-xenococcine trophobiont and/or potential trophobiont species of Acropyga ants, related co-evolution and co-speciation analyses and behavioral ecological studies may provide new insights into the evolution and maintenance of this unique obligate mutualism.