Contribution to the knowledge of Neanurinae of Vietnam with description of three new species (Collembola, Neanuridae)

Abstract Detailed and illustrated descriptions of three new species belonging to the tribe Lobellini from Vietnam are given. Lobellina weinerae sp. n. is the most similar to L. minuta (Lee, 1980) and L. musangensis Yosii, 1976, but differs from them in chaetotaxic details and the number of mandibular teeth. Lobellina pomorskii sp. n. differs from L. perfusionides (Stach, 1965) in chaetotaxic details and the number of tubercles on Abd.V. Yuukianura deharvengi sp. n. is superficially similar to Y. halophila Yosii, 1955, but it differs in the build of the maxilla, the size of eyes and an inner tooth on the claw, and in chaetotaxic details. Furthermore, some remarks on the characteristics and the peculiarity of the Vietnamese fauna of the subfamily, and the key to all species from the country, are included.


Introduction
Vietnam, in spite of its relatively small area (ca. 320,000 km 2 , 65 th in the world), is commonly known for its unique and extremely high biological diversity. This extraordinary level of biodiversity is associated with several factors, like the notable altitudinal gradient, the extreme north-south extension (8°N -24°N), the geological complexity, the absence of larger catastrophic events in the Cenozoic Era, the tropical or subtropical climate, and the presence of precious remnants of many natural environments. Nonetheless, regarding research on the fauna, the country is among the most underrepresented on the continent. The knowledge of many groups of animals in Vietnam, especially invertebrates, seems to be still in an initial phase. One of such poorly known groups are undoubtedly springtails (Collembola) belonging to primitive and wingless Hexapoda. Among Collembola living in tropics, members of the subfamily Neanurinae are probably most spectacular and conspicuous due to their relatively large body size and vivid colours.
The study of Vietnamese Neanurinae has improved notably during the two last decades, with several new taxa described and recorded from both the southern and the northern parts of the country (Nguyen Tri Tien 1995, Deharveng and Smolis 2002, Smolis and Deharveng 2003, 2005, 2006a, b, Smolis 2007. At present, considering old (Denis 1934, 1948, Stach 1965 and new contributions, the fauna of the subfamily in the country includes 18 species classified into 3 tribes (Neanurini, Paleonurini, and Lobellini) and 12 genera, namely: Neanura MacGillivray, 1893; Vietnura Womersleya Denis, 1948;Rambutanura Deharveng, 1988;Blasconura Cassagnau, 1983;Vitronura Yosii, 1969;Pronura Delamare Deboutteville, 1953;Paleonura Cassagnau, 1982;Paralobella Cassagnau & Deharveng, 1984;Lobellina Yosii, 1956;Sphareonura Cassagnau, 1983;and Deuterobella Yoshii & Suhardjono, 1992. In the present contribution, three new species of Lobellini are reported, from one of the six tribes established within the subfamily (Cassagnau 1989). This large tribe currently encompasses more than 130 species and 15 genera, distributed primarily in the Oriental and the Australian regions (Bellinger et al. 2017). The Lobellini are defined by the following combination of features: the presence of 3+3 eyes or the ocelli absent, four labral chaetae positioned in two rows, the absence of a blue hypodermic pigment on the body, the separateness of tubercles An and Fr on the head, and a bilobate last abdomen (Cassagnau 1983, 1989. Two new species, presented in this paper, belong to the genus Lobellina Yosii, 1956, while the third one to Yuukianura Yosii, 1955. Their detailed descriptions and suggestions about their close affinities are included. Additionally, general remarks on Vietnamese Neanurinae and a key to all species from the country are provided.

Materials and methods
The specimens were cleared in potassium hydroxide and chloral phenol, then mounted on slides in Swan's medium (distilled water, chloral hydrate, glacial acetic acid, glucose, Arabic gum) and studied using a Nikon Eclipse E600 phase contrast microscope. Figures were drawn with camera lucida and prepared for publication using Adobe Photoshop CS3. Terminology for the description follows that of  with rationale for the definition of chaetae categories), Deharveng and Weiner (1984), Greenslade and Deharveng (1990), Smolis and Deharveng (2006) and Smolis (2008). Chaetal morphology (Figs 1, 8). Dorsal ordinary chaetae of four types: Ml, Mc, me, and mi. Macrochaetae Ml moderately long, thin, straight, narrowly sheathed, smooth and pointed at apex. Macrochaetae Mc morphologically similar to long macrochaetae, but shorter. Mesochaetae similar to ventral chaetae, thin, smooth, and pointed. Microchaetae similar to mesochaetae, but apparently short. S-chaetae of tergites thin, smooth, and slightly shorter than nearby Ml.

Abbreviations used in text, tables and figures
Antennae (Figs 2, 3; Table 1b). Typical of the genus. S-chaetae of Ant. IV of medium length and moderately thickened. Apical vesicle trilobed. Sensillum sgd shorter and thinner than S-chaetae, not migrated distally.
Ventral chaetotaxy (Tab. 1c). On head, groups Vea, Vem and Vep with 4, 3, 4 chaetae respectively. Group Vi on head with 6 chaetae. On Abd. IV, furca rudimentary without microchaetae. On Abd. V, chaeta Vl present. Male without modified chaetae.   Remarks. As presently understood the genus Lobellina includes 13 species distributed mostly in East and Southeast Asia (Deharveng and Weiner 1984, Ma and Chen 2008, Wang et al. 2006. Interestingly, five of all known species were described from the Korean Peninsula (Lee 1980, Deharveng andWeiner 1984). Lobellina weinerae sp. n. is morphologically most similar to L. minuta (Lee, 1980) (from South Korea) and L. musangensis Yosii, 1976 (from Malaysia), resembling those species in having smooth body macrochaetae, similar length of body, tubercle Oc with 2 chaetae on head and Abd. V with 2+2 tubercles. Nevertheless, they are readily distinguished by a number of characters: body color alive (in weinerae yellow, in minuta red, in musangensis unknown), presence/absence of chaeta O on head (in weinerae present, in minuta and musangensis absent), number of mandibular teeth (in weinerae 7, in minuta 5, in musangensis 8), number of chaetae Di on Th. II-III (in weinerae 3, in minuta and musangensis 2), number of ordinary chaetae De on Th. II-III (in minuta 4, in weinerae and musangensis 3) and number of chaetae Di on Abd. V (in minuta 3, in weinerae and musangensis 2).
Etymology. The species is named in honour of Prof. Romuald Jacek Pomorski who has contributed so very much to the knowledge of Collembola.
Remarks. Taxonomy of the genus Yuukianura is controversial and problematic mostly due to insufficient descriptions of some species (Deharveng et al. 2017). The majority of species live in littoral zones of streams and seashore of many Pacific regions, from Russian Far East to Hawaiian Island and North Australia. Yuukianura deharvengi sp. n. seems to be most similar to Y. halophila Yosii, 1955, found in the Nakanoshima Island belonging to the Ryukyu Archipelago (Southern Japan). They differ in a few  subtle but distinctive and important features: shape of maxilla (in deharvengi with one ciliated lamella, in halophila lamellae without cilia), size of eyes (in deharvengi small, with diameter not longer than twice of diameter of closest granules; in halophila large, with diameter at least three times longer than diameter of closest granules), number of chaetae Di on Abd. IV (in deharvengi 3 chaetae, in halophila 2 chaetae), number of tubercles on Abd. V (in deharvengi 2+2, in halophila 1+1 tubercles), and position and size of inner tooth on claw (in deharvengi small and situated in one third of inner edge, in halophila large and in half of inner edge).

Discussion
Presently, the Neanurinae fauna in Vietnam includes 21 species in the following genera: Neanura MacGillivray, 1893 -1, Vietnura -1, Womersleya Denis, 1948-1, Rambutanura Deharveng, 1988-2, Blasconura Cassagnau, 1983-3, Vitronura Yosii, 1969-2, Pronura Delamare Deboutteville, 1953-2, Paleonura Cassagnau, 1982-2, Paralobella Cassagnau & Deharveng, 1984-1, Lobellina Yosii, 1956-3, Sphareonura Cassagnau, 1983-1, Deuterobella Yoshii & Suhardjono, 1992-1 and Yuukianura Yosii, 1955, the Vietnamese fauna of this subfamily is expected to be surely much richer and can include at least 100 taxa. This potential number seems to be likely and adequate to the biological diversity of Vietnam and the knowledge of the subfamily in other Asian countries. For comparison, the Neanurinae fauna of North Korea, a country nearly three times smaller than Vietnam and located far norther, currently comprises 23 species (Deharveng and Weiner 1984). Despite the still initial phase of the knowledge of this subfamily in Vietnam, a comparison with the data on the Neanurinae diversity in other countries, well or similarly documented in this respect, in East Asia (e.g. North Korea, China) and Southeast Asia (e.g. Thailand, Malaysia) indicates many similarities between these areas but also some peculiarities of Vietnam's fauna. These similarities are strongly manifested in the presence of many genera, e.g. Blasconura, Vitronura, Pronura, Paleonura, Paralobella, Lobellina, Sphareonura, Deuterobella, Yuukianura and Rambutanura, widely distributed and common in East Asia or Southeast Asia, or both. Interestingly, Vietnam has some of the most spectacular Neanurinae known, members of the genus Rambutanura. This genus, probably endemic for Southeast Asia, currently contains four species: R. dawydofii (Denis, 1934) (from Vietnam), R. malayana (Yosii, 1976) Deharveng, 1988 (Thailand) and R. carcharia Smolis, 2007 (Vietnam). Most Neanurinae taxa are small to medium-sized, reach maximum 2.5 mm in length, and are rather drab in color. Rambutanura, however, is much larger (up to 7 mm), more colorful, and its body is covered by numerous extremely long finger-like projections. Additionally, these unusual springtails can also be interesting for the whole scientific community, because R. yoshianna is characterized by extremely large polytene chromosomes in its salivary glands (Deharveng 1988).
The largest peculiarities in the Neanurinae fauna of Vietnam are the Vietnura genus and the species of Pronura pomorskii Smolis & Deharveng, 2006. Biogeographically, Vietnura is one of the most interesting genera in the world, as the localities of V. caerulea  are the most southern (12° N) records of Neanurini . Until its discovery, excluding a few Neanurini species introduced by humans outside their natural range limit, this large and diversified tribe was known exclusively from the Palearctic and Nearctic Regions (e.g. Fjellberg 1985, Babenko and Fjellberg 2006, Deharveng et al. 2015, Mayvan et al. 2015. Pronura pomorskii, in turn, is unique among all Neanurinae due to presence of tubercles on the border between terga; normally, if present, these cuticular structures are located on tergites only (Smolis and Deharveng 2006a).
Considering the present stage of knowledge on Neanurinae, notable absences from the Vietnamese fauna are Paranura Axelson, 1902, Siamanura Deharveng, 1987and Blasconurella Deharveng & Bedos, 1992, genera that are species-rich and widespread on the continent. Nevertheless, as the fauna of Vietnam becomes better explored, we will probably discover these speies also there and see more similarities with the adjacent countries' fauna. It is also likely that most of the described species will be endemic to the country. To sum up, a great deal of work is needed regarding the taxonomy of this group in the country, particularly to describe the unknown diversity, sort out the taxonomy, and resolve relationships among the species.

Key to Neanurinae species from Vietnam
The key is based partially on Deharveng and Bedos (2000). It should be noted that the published records of some taxa from Vietnam are not well-documented (species marked below by asterisks); therefore, they are in need of verification and confirmation.