New record of Didymocorypha Wood-Mason (Mantodea, Eremiaphilidae) from China, with description of a new high-altitude wingless mantis species in Asia

Abstract The genus Didymocorypha Wood-Mason, 1877 (Eremiaphilidae, Iridinae) has only been recorded in South Asia, including a sole species D. lanceolata (Fabricius). Here, we firstly extend its distribution to China, with description of one new species D. libaiisp. nov.Didymocorypha libaiisp. nov. lives in an area about 3000 meters above sea level on the southern slope of the Himalayas (Tibet in China), one of the highest-altitude inhabited areas of mantis in the Northern Hemisphere. It is also the first recorded Oriental mantis species in which both sexes are wingless. Life history of the new species, necessary illustrations and ecological images are provided. The distribution of the new Didymocorypha species is discussed and mapped.


Introduction
The genus Didymocorypha was erected for a sole species D. ensifera Wood-Mason, 1877 from Sri Lanka with which Pyrgocotis gracilipes Stål, 1877 was synonymized (Wood-Mason 1882). Subsequently, Mantis lanceolata Fabricius, 1798, which was recorded from Eastern India, was transferred into the genus Didymocorypha by Bolivar (1897). Afterwards, D. ensifera was considered as a synonym of D. lanceolata (Kirby 1904). At the time of Ehrmann's catalogue (Ehrmann 2002) the genus Didymocorypha only possessed one species, D. lanceolata, which is widely distributed in South Asia (e.g., Sri Lanka, Nepal and India). In Schwarz and Roy's (2019) new taxonomic system, the genus Didymocorypha belongs to subfamily Iridinae (Eremiaphilidae). This subfamily includes eight genera, among which seven range from Africa to South Asia and one genus Iris Saussure ranges from Africa and Europe to northwestern China (Wang 1993). Until now, no other genera of the subfamily Iridinae or the family Eremiaphilidae have been recorded from China.
Within the order Mantodea, brachypterous females are common. Apterous females are a rarity except in some families, for example Thespidae and Haaniidae. It is also rare that both sexes of a certain species are wingless. As far as we know, both sexes are apterous in three Old World mantis genera, Apteromantis Werner, 1931 (Amelidae), Geomantis Pantel, 1896 (Rivetinidae), Holaptilon Beier, 1964 (Gonypetidae), one African genus Apterocorypha Roy, 1966 (Hoplocoryphidae) and one North American genus Yersiniops Hebard, 1931 (Amelidae) (Ehrmann 2002;Battiston et al. 2010). Most of these apterous mantis species are small-sized, and live in grassland or shrubland in temperate regions. No mantis species with apterous males and females has been recorded within the family Eremiaphilidae or in the Oriental Realm.
When investigating fauna on the southern slope of the Himalayas in Tibet, China, we collected apterous adult specimens of Didymocorypha from Gyirong County at an altitude of 3000 meters in 2017. After dissecting the male specimens and comparing them with Indian samples of D. lanceolata, we thought that those wingless specimens should belong to a unique new species of Didymocorypha. The new species is the first recorded species of Didymocorypha from China, and the first recorded Oriental mantis species with wingless male and female adults. Didymocorypha is the second recorded genus of the family Eremiaphilidae from China. Here, we review the genus Didymocorypha, provide a redescription of the known species, and thoroughly describe the new species and its life history.

Material and methods
Classification system follows Schwarz and Roy (2019). Descriptive terminology of adult morphology and the male genitalia follows Brannoch et al. (2017) and Schwarz and Roy (2019). All specimens of the new species were collected during daytime through careful observation. Genitalia were dissected in 10% KOH solution, cleared with pure water, and finally stored in 70% ethanol in Eppendorf tubes for further research. Pictures were taken with a Nikon digital camera.
The specimens were deposited in the following institutions or private collections.

Taxonomic treatment
Didymocorypha  (Fig. 4), with lateral lobes of vertex prolonged into triangular processes, running alongside each other but not fused. Compound eyes large, oblong. Lower frons approximately trapezoid. Pronotum slender, with nearly parallel lateral margins. Fore legs weak. Fore femur (Fig.  5A, B) with 4 ventro-posterior and 4 discoidal spines; claw groove in the middle; fore tarsus much longer than tibia, and basal tarsomere longer than total length of remaining segments. Middle and hind legs slim without expansions but with genicular spines. Hind legs longer and stronger than mesolegs, similar to jumping legs of locusts. Male winged ( Fig. 1A)  Description. Male. Slim and slender, withered-grass-like (Fig. 1A). Three ocelli large and hump (Fig. 4A). Fore femur approximately as long as fore coxa, with 4 posteroventral, 4 discoidal, 17 anteroventral spines; claw groove lying basally than middle of fore femur. Fore tibia about half as long as femur, with 5 posteroventral, 10 anteroventral spines and 1 strong tibial spur. Wings hyaline and iridescent, a little shorter than body; fore wings long and narrow, hind wings broad. Cerci flat, wide, lanceolate, with distal joints gradually becoming longer distad (Fig. 5C).   External genitalia (Fig. 6A) small; left phallomere narrow, long, with finger-like process paa and about 12 thick bristles on the afa; ventral phallomere with a robust short sharp spd.
Thorax: pronotum longer than head, slender, about 3 times as long as wide. Prozona almost as wide as metazona. Mesothorax similar to metathorax, simple, nearly trapezoidal. Thorax with distinct medial keel. Wingless.
Meso-and metathoracic legs: slim without expansions and with one small femoral genicular spur and one obvious tibial spur. Tarsus much shorter than tibia; basal tarsomere short, less than total length of remaining segments. Metathoracic legs longer and stronger than mesolegs.
External genitalia (Fig. 6B, C): relatively large-sized. Left phallomere narrow and long, posterior process of ventral phallomere (spd) indistinct; phalloid apophysis (afa) short, wide and strongly sclerotized, with a spine-like projection; posterior process of left phallomere (paa) with a finger-like extension, with a small obtuse tubercle in middle, and with a brush-like cluster of hairs on base.
Diagnosis. The new species is distinguished from D. lanceolata by small body size, small and indistinct male ocelli, wingless male adults, comparatively large-sized genitalia, ventral phallomere without secondary distal process (sdp), additional obtuse tubercle on paa and different structure of afa (Fig. 6).
Life history. The new species often lives at the bottom of bushes in a variety of angiosperms (Figs 2, 3A-D) in high-altitude coniferous forest. Nymphs were found to be clustering (Fig. 3B), without cannibalism. This peaceful situation is an exception for mantis. The mating (Fig. 3D) is also peaceful, and needs up to 4-8 hours. Female lays their oothecae on the fifth day after mating. Oothecae are fusiform, withered-leaf-like. Each ootheca contains 4-10 eggs (Fig. 1D). Color of ootheca varies from light to very dark brown. External wall of cotheca is thin, sparse. Oothecae did not hatch successfully in the laboratory probably due to significant elevation differences from the mantis's natural habitat. In field, the mantis species prey on small-sized insects (e.g., Diptera, Hemiptera and Collembola) (Fig. 3C), based on our observations. Distribution. China (Tibet: Gyirong County). Etymology. The new species was named after Bai Li, who is a poet in the Tang dynasty of China and one of the most famous poets in Chinese history.

Discussion
Didymocorypha libaii sp. nov., is the first mantis species recorded at altitudes of more than 3000 meters (Fig. 3E) in China. At the type locality of D. libaii sp. nov., blankets of snow persist during the long winter, and the growing period is very short. In fact, it was difficult to distinguish the adults and nymphs of this new species from each other in general appearance. Initially, we judged them to be adults because they were mating when breeding indoors. Retention of nymph characteristics in the adults is called neoteny. We assume in the harsh environment of type locality of D. libaii sp. nov., that neotenic development could help to shorten the life cycle of the mantis, simultaneously, the large-sized male genitalia of the species can improve the success rate of copulation. In summary, the wingless adults and the large-sized male genitalia enable the species to adapt to the harsh environment.
We suppose that the new species was isolated by the uplifted Himalayas and diverged from its congener. Its ancestral population adapted to the environment at high altitudes, and was restricted to a very narrow range. In addition, a few mantis species (of genera Arria Stål, 1877, Odontomantis Saussure, 1871 and Phyllothelys Wood-Mason, 1877) are also found at an altitude of about 2500 m in China (including high-altitude areas of the Himalayas) based on our collections, which we will report in other papers. There are a range of suitable environments on the southern slopes of the Himalayas in China and more discoveries will possibly be made in the future.
The other recorded mantis species at high altitude include Pseudopogonogaster hebardi (Terra, 1982) from Ecuador at elevations 3500 m and Armene breviptera Lindt, 1963 from Badakhshan (West Pamir Mountains) at elevations 2300-2700 m. One ootheca of A. breviptera was even found at 3700 m (Lindt 1963). Armene breviptera was the only species of Mantodea that was previously found in the harsh environment. The dominant ecosystem there is dry mountain grassland with short and sparse vegetation cover, without trees or bushes and with very low biodiversity comparing to the lower elevations in the same region. The snow cover during winter is intermittent and often does not provide sufficient thermal protection during the cold months (Khakimov et al. 2007). Armene breviptera is the only micropterous species in the genus, also suggesting a connection between harsh external conditions and wing adaptation in Mantodea. By comparison, Didymocorypha libaii sp. nov. lives in a significantly milder environment with abundant vegetation, including trees, in spite of long winters. The conditions of D. libaii are also atypical for Mantodea also suggesting possible adaptations of the species to the short growth period.