A Remarkable New Genus and New Species of the Plant Bug (Heteroptera: Miridae: Phylinae), Inhabiting Psyllid Leaf Margin Roll Gall on Indian Banyan, Ficus benghalensis

ABSTRACT A new genus and new species of the plant bug, Chimairacoris lakshmiae Yasunaga, Schuh, and Cassis are described from Bangalore, India. This morphologically and ecologically specialized mirid belongs to the subfamily Phylinae on the basis of genitalic structures and is currently considered best placed in the subtribe Oncotylina of the tribe Phylini. Its morphological convergence with termatophyline mirids and placement within the Phylinae are discussed. It is associated with psyllid leaf galls on Indian banyan, Ficus benghalensis. The gall-producing psyllid, Trioza sp., and a mealybug, Phenacoccus parvus, are confirmed as prey of this unique mirid. A similar phenomenon observed in some Montandoniola spp. (Anthocoridae) and Fingulus species (Miridae: Deraeocorinae), which are associated with thrips species of the genus Gynaikothrips (Thysanoptera: Tubulifera) on Ficus microcarpa, is also documented.


INTRODUCTION
This work reports the discovery of a morphologically and ecologically remarkable plant bug, representing a new genus and a species of the subfamily Phylinae from Bangalore, South India. Although the external appearance of this mirid resembles that of members of the tribe Termatophylini (Deraeocorinae), the male and female genitalic structures unequivocally place it in the Phylinae. Furthermore, the shape of the external metathoracic scent-efferent system is very similar to that found in certain species of Anthocoridae and the rather toughened body with the shortened legs and expanded abdomen beyond the corial margin is structurally similar to that seen in the Thaumastocorinae. The nymphal stages are also specialized, and have rhyparochromid-like facies (Lygaeoidea) because of their red and black coloration.
The new species can be found inside of leaf-margin roll galls produced by a psyllid (Trioza sp.) on the Indian banyan (Ficus benghalensis L.). The mirid was observed to prey not only on the psyllid but also on a mealybug, Phenacoccus parvus Morrison, which often cooccurs on the same individual banyan tree. Because of its unusual, concealed habitat preference, such a conspicuous bug, in spite of existing so close to humankind, had been ignored until very recent field investigations discovered it.
We herein describe a new genus, Chimairacoris, to accommodate this peculiar, predaceous, new mirid species. We discuss its suprageneric position, offering reasons why we place it in the tribe Phylini of the Phylinae. The similarity of habitat and food preferences with those observed in species of the genus Montandoniola (Anthocoridae) and Fingulus spp. (Miridae: Deraeocorinae) is also discussed.

MATERIALS AND METHODS
All examined specimens were collected by P.J. and her colleagues, who also made all of the field observations. Type materials are deposited in the following collections: Matrix-code labels are attached to most adult specimens, which uniquely identify those specimens, and are referred to as unique specimen identifiers (USIs). The USI codes (e.g., AMNH_PBI 012345) comprise a data set code (AMNH_PBI) and a unique specimen number (e.g., 012345). These data were digitized on the Planetary Biodiversity Inventory instance of the Arthropod Easy Capture database of the AMNH (http://research.amnh.org/pbi/) and are distributed online (http://www.discoverlife.org and http://research.amnh.org/pbi/heteropteraspeciespages).  5): Vestibular sclerites asymmetrical, enlarged, projecting to right hand side; seminal depository large; sclerotized rings distinctly rimmed, ovoid; interramal sclerite thin; ramus toughened, with an inner, triangular process anterodorsally.
Etymology: From Greek (mythology), Chimaira (Χίμαιρα = chimera, a fictitious animal composed of lion head, goat body, and dragon tail) combined with coris (κόρις = bug), referring to its nearly termatophyline body shape, with anthocorid-shaped metathoracic scent efferent system, typical phyline-type genitalia, and rhyparochromid-like coloration in immature forms; gender masculine. Discussion. This remarkable new genus is readily distinguished from all other phyline genera by the characters listed above. We regard its flattened body and short appendages as adaptations for inhabiting narrow spaces in leaf roll galls (see species description for biology).
The following structural features found in Chimairacoris are unusual in the Miridae but (sometimes commonly) known in other family groups: scent-efferent system as in figures 3B and 4A, without noticeable pore, cleft, or concave gland opening (most similar to Anthocoridae); strong spines on broadened profemur, possibly useful for predation (Anthocoridae, Nabidae, Reduviidae, Plokiophilidae, Pyrrhocoridae, etc.); very short tibia as long as respective femur, as in some species of anthocorid genus Scoloposcelis Fieber (Anthocoridae) that often inhabit narrow spaces under bark of rotten logs; developed metafemoral spines, which are also unusual in most heteropteran families, but some leaf-footed bugs (Coreidae) are equipped with metafemoral spines that are assumed to be used for conflict or defense; widened abdomen beyond lateral margins of hemelytron, which is frequently found in many groups of the Heteroptera but usually not prominent in most mirid bugs (for further information on other heteropteran families, see Schuh and Slater, 1995).
Some of the morphological features of Chimairacoris are reminiscent of those found in termatophyline mirids and anthocorids (Cassis 1995), and at first we thought our new taxon was a termatophyline mirid. Chimairacoris and termatophylines (and also some deraeocorines, e.g., Fingulus as in fig ). The Termatophylini are also characterized by the following distinctive characters: pronotum and veins and fractures of hemelytron with patterned rows of punctures, pretarsal claw with basal tooth and without pulvilli, and endosoma simple, with indiscernible secondary gonopore (Cassis, 1995). Chimairacoris lacks all of these characters, which brought into question our thought that it belonged to the Deraeocorinae. In addition, the compound eye is smaller, and has flattened, rather irregularly arranged ommatidia, and lacks any sensory setae, features that are common in termatophylines and many other mirids.
There is apparent convergence in habits and habitats of Chimairacoris and some termatophyline species (10 genera, 35 species; Cassis, 1995;Schuh, 2002Schuh, -2014. Several termatophylines are found on inflorescences of broadleaf angiosperms (cf. fig. 7G), and often observed to feed on nectar and/or pollen although they appear predominantly to prey on thrips or other tiny arthropods (Yasunaga et al., 2001). In contrast, other termatophylines are known from concealed habitats, such as moth larval galleries and rolled bark (Cassis, 1995;Cassis et al., 2011), and are assumed to be predators. In addition, the short first labial segment of Chimairacoris and termatophylines is apparently indicative of a predatory habit.
The male and female genitalia are one of the most important character systems for determining the systematic position of mirid taxa (Schuh and Slater, 1995;Cassis and Schuh, 2012). Our investigation of these character systems in Chimairacoris both surprised us, and left us in no doubt that this taxon belongs to the subfamily Phylinae. In particular, the structure of the endosoma, placement of the secondary gonopore, attachment of the phallotheca to pygophore, and the shape of the parameres are defining characters for the Phylinae and allow us to conclude that any similarities with Chimairacoris and termatophylines are due to convergence.
Thus, even though there is little doubt about the placement of Chimairacoris within the Phylinae (see Schuh and Menard, 2013, for current classification), we are less certain about its tribal/subtribal position. On the basis of the slender, J-shaped endosoma and subapical secondary gonopore, Chimairacoris resembles Brachyarthrum Fieber and Phymatopsallus Knight of the subtribe Oncotylina. On the other hand, its well developed and somewhat sigmoid female vestibular sclerites are found in representatives of several phyline tribes (e.g., Atractotomoidea Yasunaga of Nasocorini, Phymatopsallus group of Phylini: Oncotylina) (Schuh, 2006;Schuh and Menard, 2013;Yasunaga, 2010), as well as in the Hallodapini (Pluot-Sigwalt and Matocq, 2006;Wyniger, 2006). Current evidence suggests possible placement of Chimairacoris in three tribes: Nasocorini, Phylini (Oncotylina), or Pilophorini. Which of the placements-if any-might prevail in the long run is unclear and will doubtless depend on the acquisition of DNA sequence data. The small size, dark coloration, and predatory habits might well suggest an association with the Nasocorini, as all those features are seen in genera such as Rhinacloa Reuter, and at least two of them are found in other nasocorine genera such as Campylomma Reuter, Spanagonicus Berg, and probably others. The triangularly developed pulvillus (at first sight similar to the deraeocorine basal claw tooth) is recognized not only in Chimairacoris but also in FIG. 5. Male genitalia of Chimairacoris lakshmiae. Apical part of pygophore cracked along the midline appears to be a result of preparation or dissection, or this part may be weakly sclerotized (cf. fig. 3F). some phyline tribes, such as Acrotelus Reuter (Oncotylina) and Macrotylus Fieber (Cremnorrhinini: Cremnorrhinina). On the other hand, the male and female genitalia possibly show greater structural similarity with the Oncotylina, particularly genera such as Phymatopsallus. There are also similarities in coloration, antennal structure, predatory habits, and small size with the New World spider-commensal genus Ranzovius Distant, which was placed in the Oncotylina by Schuh and Menard (2013).
It is our opinion that comparison with Pilophorini also merits careful consideration. This is a group that almost certainly shows some tendency toward predation in many species, even though the evidence for this is largely inferential. Also, the slender, tubular, J-shaped endosoma in Chimairacoris strongly resembles many members of the Pilophorini, as does the dark coloration and elongate, nearly parallel-sided body form. Compare Chimairacoris with Pilophorus gracilis Uhler, for example. Nevertheless, Pilophorini, as diagnosed by Schuh (1974Schuh ( , 1984, do not have a sclerotized secondary gonopore, but the work of Schuh and Menard (2013) and Menard et al. (2014) indicates that the situation is more complex than previously thought, revealing that the Pilophorini lineage includes taxa that have a broader range of setal types than previously thought to be the case, that the pretarsus is not monolithic in its structure and can vary from the classic Pilophorus Hahn type, and that members of the lineage may also have a sclerotized secondary gonopore (Lasiolabops Poppius), all features not seen in the group as conceived by Schuh (1974Schuh ( , 1984. The preponderance of the evidence argues for the placement of Chimairacoris in the Oncotylina. Diagnosis: This species is recognized by the generic diagnostic characters; no other known phyline species exhibits them. Nymphs, (figs 1B, 2C, D) superficially similar to those of some cylapine mirids (e.g., Fulvius spp.) or lygaeoids (e.g., Rhyparochromidae), can be recognized by the elongate body, densely distributed, short, stiff setae on dorsum, generally dark bluish coloration, somewhat reddish head, and red anterior half of the abdomen.
Description: Coloration: Body generally fuscous, partly shining, velvety or roughened (figs. 1A, 2A). Eye dark red. Extreme apex of antennal segment II, entire III and basal half of IV yellow. Labial segments II and III pale brown. Hemelytral membrane grayish brown, semitransparent. Coxae partly pruinose or shagreened. Apex of all femora and tibiae, and entire tarsus yellowish brown. Abdomen entirely fuscous. Structure: As in generic description. Pronotum posterior to calli, scutellum, and hemelytron shallowly, roughly and irregularly punctate. Pleura and basal part of all coxae partly shagreened or roughened.
Distribution: South India (Bangalore). Biology: Although the present new species exists close to human settlement, it was not until quite recently that this intriguing bug was discovered by one of the authors (P.J.) and her eager colleagues, due to its concealed and unexpected habitat preference.
Chimairacoris lakshimiae inhabits the leaf-margin roll galls produced by Trioza sp.

E−G). This
Trioza species folds and tightly rolls one or both margins of the banyan leaves, and the nymphs remain sheltered inside these roll galls, which are often covered with globules of honeydew. A mealybug, Phenacoccus parvus Morrison (Sternorrhyncha: Pseudococcidae), is also commonly found with the psyllids in the same galls ( fig. 1I). A possibly undescribed species of the genus Anthocoris Fallén (Anthocoridae) is observed to cooccur in the same niche (Poorani and Yamada, unpublished data). In India, Yamada et al. (2011) also reported that eggs, all immature stages, and adults of Montandoniola indica Yamada (Anthocoridae: Oriini) inhabit the leaf curl galls induced by the thrips, Liothrips karnyi Bagnall (Phlaeothripidae) on leaves of black pepper, Piper nigrum L. (Piperaceae).
Chimairacoris lakshmiae was observed to deposit eggs in small groups in the leaf roll galls. The eggs are embedded into the leaf tissue ( fig. 1 C), with the opercula exposed on the gall surface ( fig. 1 D). The nymphs are always found inside the galls where they apparently complete their life cycle. All developmental stages were seen throughout the year and as a result we assume that C. lakshmiae is multivoltine. In Bangalore peak populations were observed during summer (May through July), which taper off in the dry winter season (December through January). The basic structure of the small compound eye appears to be rather simple and rougher than that of other mirids; the ommatidia are flat and not so evenly arranged. Chimairacoris lakshmiae completes its whole life cycle in the dark gall, which implies the visual function of this species might be somewhat regressed, or unneeded for this bug.
A similar life style is confirmed in species of the flower bug genus Montandoniola Poppius (Anthocoridae); some species are known to be associated with leaf roll (or curl) galls produced by thrips, Gynaikothrips spp. (Thysanoptera: Tubulifera), on Ficus microcarpa L.f., and the anthocorids propagate and prey on the thrips in and around the galls (fig. 7A−E) (Tavaresa et al., 2013;Yamada et al., 2010;Yasunaga et al., 2001). The adults of these anthocorid bugs putatively mimic the thrips upon which they prey (cf. fig. 7D and E). However, these anthocorids appear to attack smaller immature thrips only, as the adult thrips (larger in size than the bug) were observed to repel the predators, wielding the long, posterior end of the abdomen when approached (Yasunaga and Yamada, unpublished observation both in Cambodia and Thailand). Mimicking host insects and inhabiting colonies with their prey may allow these predaceous bugs to minimize the threat of natural enemies, as supposed by Yasunaga et al. (1997Yasunaga et al. ( , 2001. Mirid species of the genus Stethoconus Flor (Deraeocorinae: Hyaliodini), which preferably attack lace bugs (Tingidae) within the tingid colonies, also probably mimics their prey (see Wheeler, 2001).
During recent observations at a college campus in Siem Reap, Cambodia, one of the authors (T.Y.) found more than a few individuals of a possibly undescribed Fingulus species (Deraeocorinae: Deraeocorini) ( fig. 7F) and some of Cardiastethus (probably) exiguus Poppius (Anthocoridae: Cardiastethini) from the leaf roll galls of Ficus microcarpa. Also in Japan Fingulus longicornis Miyamoto is known to have a close association with the gall of Ficus microcarpa made by its assumed prey, Gynaikothrips ficorum (Marchal) (fig. 7E); the late instar immatures of this mirid have an elongate abdomen and are similar in appearance to (and probably mimetic of) the thrips (Nakatani et al., 2000;Yasunaga et al., 2001). Incidentally, fruits of Ficus microcarpa, F. superba (Miq.) Miq. and F. religiosa L. serve as a breeding site for the phytophagous pilophorine, Lasiolabops cosmopolites Schuh. In tropical and subtropical zones of Asia, little is currently known about the faunas of both gall-making insects and their heteropteran predators on Ficus trees. Further studies on the faunas and their biology are required to demonstrate their coevolution as well as any remarkable morphological modifications similar to those seen in Chimairacoris lakshmiae. Since the present document is based upon surveys targeting a few plant species for landscaping or worship within rather artificial or urbanized zones, more unexpected, morphologically or ecologically novel species may be discovered from well-preserved environments.