Collembola: Tomoceridae

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Two new species of Pogonognathellus (Collembola: Tomoceridae) from China, with a discussion of East Asian species a

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Tianle Wang , Daoyuan Yu & Feng Zhang

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School of Life Sciences , Nanjing University , Nanjing , China Published online: 18 Mar 2013.

To cite this article: Tianle Wang , Daoyuan Yu & Feng Zhang (2013) Two new species of Pogonognathellus (Collembola: Tomoceridae) from China, with a discussion of East Asian species, Journal of Natural History, 47:17-18, 1243-1255, DOI: 10.1080/00222933.2012.752541 To link to this article: http://dx.doi.org/10.1080/00222933.2012.752541

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Journal of Natural History, 2013 Vol. 47, Nos. 17–18, 1243–1255, http://dx.doi.org/10.1080/00222933.2012.752541

Two new species of Pogonognathellus (Collembola: Tomoceridae) from China, with a discussion of East Asian species Tianle Wang† , Daoyuan Yu† and Feng Zhang* School of Life Sciences, Nanjing University, Nanjing, China

Downloaded by [Nanjing University] at 23:40 10 March 2014

(Received 27 April 2012; final version received 17 October 2012; first published online 18 March 2013)

Thirteen species of the genus Pogonognathellus Paclt, 1944 have been reported worldwide, two from East Asia. Two new species of the genus from Jilin Province, northeast China are described here. Pogonognathellus heterochros sp. nov. is characterized by its unique body colour. Pogonognathellus mai sp. nov. is most similar to Pogonognathellus beckeri (Börner, 1909) but differs from it mainly in maxilla and tenaculum. A key to the East Asian species is provided, and the confusion among these species is discussed. http://www.zoobank.org/urn:lsid:zoobank.org:pub:902CD044-0A58-4CCF-A1B1449C9DE10938 Keywords: Pogonognathellus heterochros sp. nov.; Pogonognathellus mai sp. nov.; Jilin, Asia

Introduction Börner (1908) established a new genus Pogonognathus by the presence of a beard-like appendix on the maxillary head. Later, Paclt (1944) found the initial generic name preoccupied and corrected it to Pogonognathellus. There have been 13 known species, most of which were originally described from North America [P. bidentatus (Folsom, 1913), P. nigritus (Maynard, 1951), P. elongatus (Maynard, 1951), P. celsus (Christiansen, 1964), P. danieli Felderhoff, Bernard, Moulton, 2010, P. mystax Felderhoff, Bernard, Moulton, 2010, P. belmontorum Park, Bernard, Moulton, 2011, P. brevifulvus Park, Bernard, Moulton, 2011, P. magnibrunneus Park, Bernard, Moulton, 2011], others from Europe [P. longicornis (Müller, 1776), P. flavescens (Tullberg, 1871)] and Japan [P. beckeri (Börner, 1909), P. borealis Yosii, 1967]. Two of these species, P. flavescens and P. longicornis, were recorded from Sichuan Province, China (Li 1987). Two new species of Pogonognathellus from Changbai Mountain, Jilin Province, China are described here. Confusion about several East Asian species is also discussed. Material and methods All specimens were collected from forest litter and rotten wood using aspirators or Tullgren–Berlese funnels, and soon transferred into 99% alcohol for preservation. After being photographed with a Nikon SMZ1000 microscope with Nikon DS-Fi1 camera, specimens were cleared in lactic acid and mounted in Marc André II solution. *Corresponding author. Email: [email protected] † These authors contributed equally. © 2013 Taylor & Francis

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The head, furcula and legs of one side were cut from the trunk and mounted separately for further observation. The mounted specimens on slides were studied using a Nikon E600 microscope. Figures were sketched by hand and enhanced with PHOTOSHOP CS4 (Adobe Inc.). Dorsal chaetotaxy was determined after Christiansen (1964). Dental spine formula follows Folsom (1913), arranging the dental spines from basal to distal, with a slash indicating the divide between basal and medial sub-segments and the roman numerals referring to spines obviously larger. Lamellae 1–6 of maxillary head were illustrated after Fjellberg (2007). All the material is deposited in the School of Life Sciences, Nanjing University, China (NJU). Abbreviations: Abd., abdominal segment; Ant., antennal segment; Th., thoracic segment.

Taxonomy Pogonognathellus heterochros sp. nov. (Figures 1A, 2–4)

Description Body length. Up to 6.9 mm. Body colour. Scales brown. Ground colour white. Ant. III, head, Th. II, base of front and mid legs dark purple. Pigment on Ant. III darker at the base and gradually lighter towards tip. Eye patches black. Unpigmented spots on Th. II forming an irregular but relatively stable pattern. Anterior part of Th. III and femora of hind legs with diffuse purple pigment (Figure 1A). Head. Antennae about 0.75 times body length, antennal length ratio as I : II : III + IV = 1.0 : 1.4 : 7.1–10.0, Ant. I, II and base of Ant. III scaled. Ommatidia 6 + 6.

Figure 1. Body size and colour pattern of specimens in alcohol. (A) Pogonognathellus heterochros sp. nov.; (B) Pogonognathellus mai sp. nov.

Journal of Natural History 1245


Labral setae four/five, five, four, all smooth, four setae of the third row thicker than others, labral margin with four spiny papillae, medial two curved and thinner, lateral two straight and stronger (Figure 2A). Left and right mandible respectively with four and five apical teeth, a strong tapered tooth present distally on left molar plate and a hollow present in place on opposite side (Figure 2B). Maxillary lamella 5 with long basal teeth, no distinct beard-like appendix observed (Figure 2C). Papilla of maxillary outer lobe with four setae, one basal, one apical and two median, the apical one much stronger; sublobal plate with four guard setae (Figure 2D). Labial palp A–E (Fjellberg 1998) with zero, five, zero, four, seven guard setae, hypostomal setae H rod-like, h1 thicker and longer than h2 (Figure 2E). Proximal, basomedian and basolateral area of labium each with about 40 setae. Dorsal chaetotaxy. Macrochaetotaxy as in Figures 2F and 3A. Dorsal head with two, four anterior and two posterior macrochaetae; 4 + 4 posterior marginal setae arranged in a loose row (Figure 2F). Macrochaetae on each tergum with one to six guard microchaetae and bothriotricha without those accessory setae around it. Abd. IV without anterior macrochaeta (Figure 3A). Legs. Trochanteral organ reduced to one, one slender spiny seta; some shorter smooth spiny setae present over a distance around trochanteral organ, sockets of them rounded and big as those of setae on trochanteral organ (Figure 3B). Tibiotarsus with zero, zero, two blunt spiny inner setae (Figure 3C). Tenent hair apically spatulate, much shorter than inner side of unguis. Unguis relatively straight, curved only at tips, with four, four, four inner teeth and a pair of pseudonychia. Unguiculus about two-thirds the length of unguis and with one inner tooth (Figure 4A). Abdominal appendages. Ventral tube covered by scales and setae both anteriorly and posteriorly; each side of anterior face with about 40 setae in different sizes, three of which larger than others. Tenaculum with 4 + 4 teeth, corpus unscaled and with one seta shorter than rami (Figure 4B). Furcula ratio as 4.3–5.0 : 5.3–6.6 : 1.0 from manubrium to mucro. Manubrium with lateral row of 11–13 large blunt setae, both dorsal and ventral face scaled and no distinct “principal setae” appearing on dorsal face. Inner bases of dentes bearing a pair of large pointed scales with a few striate sculptures on surface. Dental spine formula as II/7–10, II. Spines all simple, with irregular longitudinal streaks, basal pair on medial dental parts distinctly smaller than others (Figure 4C). Mucro elongate, basal two teeth close to each other, distance from base of mucro to inner basal tooth about 1/12 length of mucro, apical and subapical teeth subequal, dorsal lamella with 6–11 intermittent teeth. Apical mucronal setae much larger than others (Figure 4D).

Types Female holotype and two female paratypes on slides and five in alcohol in NJU. Location: Erdaobaihe Town, Antu County, Yanbian Korean Autonomous Prefecture, Jilin Province, China. In forest litter. Collected by CHEN Jianxiu, MA Yitong and YU Daoyuan.


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Figure 2. Pogonognathellus heterochros sp. nov. (A) Labrum; (B) mandible; (C) maxillary head (1–6: lamella 1–6); (D) maxillary outer lobe; (E) hypostomal setae in labial pulp; (F) dorsal cephalic macrochaetotaxy.



Figure 3. Pogonognathellus heterochros sp. nov. (A) Dorsal tergal macrochaetotaxy; (B) trochanteral organ; (C) spiny inner setae on hind tibiotarsus.


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Figure 4. Pogonognathellus heterochros sp. nov. (A) Claw; (B) tenaculum; (C) dental spines; (D) mucro.

Journal of Natural History 1249 Etymology Named for its unique cuticular colour. Greek word hetero for different, chros for pigmentation.


Remarks Pogonognathellus heterochros sp. nov. is similar to P. flavescens in details, such as unguis, dental spines and mucro, but it lacks the long beard-like appendix at the base of maxillary lamella 5, which is a significant character in P. flavescens (Yosii 1967; Fjellberg; 2007; Felderhoff et al. 2010). This new species can be easily recognized by the unique body colour in alcohol. Pogonognathellus mai sp. nov. (Figures 1B, 5, 6, 7)

Description Body length. Up to 3.4 mm. Body colour. Scales brown. Ground colour yellow. Ant. III and IV light brown, darker at tips. Eye patches black and pigment expanding to encircling antennal bases. Venter of Th. I and base of front legs dark blue. Base of mid and hind legs diffusely pigmented (Figure 1B). Head. Antennae short, about half the length of body, antennal length ratio as I : II : III : IV = 1.0 : 1.7 : 6.5–7.3 : 1.3. Ommatidia 6 + 6. Labral setae four/five, five, four, distal four thicker, four marginal papillae with rather blunt tips, lateral two slightly stronger than medial ones (Figure 5A). Molar plates distally with tapered tooth on the left one and hollow on the right one (Figure 5B). Maxillary beard-like appendix not distinct (Figure 5C). Dorsal chaetatoxy. Macrochaetotaxy as in Figures 5D and 6A. Dorsal head with two, four anterior and two posterior macrochaetae, and 4 + 4 posterior marginal setae (Figure 5D). Tergal macrochaetae with, but bothriotricha without, guard microchaeta. Anterior macrochaeta on Abd. IV absent (Figure 6A). Legs. Trochanteral organ reduced to one, one slender spiny setae. Tibiotarsal blunt setae as zero, zero, two (Figure 6B). Tenent hair shorter than inner side of unguis, apically spathulate. Unguis curved, with four, four, four inner teeth, pseudonychia well developed. Unguiculus with one inner tooth (Figure 6C). Abdominal appendages. Ventral tube covered by scales and setae both anteriorly and posteriorly, each side of anterior face with about 30 setae, three of which larger than others (Figure 7A). Tenaculum with 4 + 4 teeth and corpus with one seta longer than rami (Figure 7B). Furcula ratio as 5.4 : 5.6–6.5 : 1.0. Manubrium scaled both dorsally and ventrally, each lateral row with 12 strong setae. Inner basal scales of dentes pointed and smooth. Dental spine formula as II/5–6, II. Spines all simple,


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Figure 5. Pogonognathellus mai sp. nov. (A) Labrum; (B) mandible; (C) maxillary head; (D) dorsal cephalic macrochaetotaxy.

with irregular longitudinal streaks, basal two pairs slender and a bit longer than terminal ones (Figure 7C). Mucro stout, basal two teeth close to each other, inner basal tooth located about one-seventh length of mucro from base, apical tooth slightly smaller than subapical tooth, dorsal lamella with five–seven intermittent teeth (Figure 7D). Types Female holotype and female paratype on slides and three in alcohol in NJU. Location: Erdaobaihe Town, Antu County, Yanbian Korean Autonomous Prefecture, Jilin Province, China. In forest litter. Collector: CHEN Jianxiu, MA Yitong and YU Daoyuan.



Figure 6. Pogonognathellus mai sp. nov. (A) Dorsal tergal macrochaetotaxy; (B) spiny inner setae on hind tibiotarsus; (C) claw.


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Figure 7. Pogonognathellus mai sp. nov. (A) Anterior face of ventral tube; (B) tenaculum; (C) dental spines; (D) mucro.

Journal of Natural History 1253 Etymology Named after Mr MA. Yitong who helped to collect type specimens.


Remarks Pogononathellus mai sp. nov. is most similar to Japanese species P. beckeri in dental spines and stout mucronal shape, but the absence of distinct beard-like appendix, the different colour pattern, one seta on corpus of tenaculum and four, four, four ungual teeth indicate that they are different. It is also similar to P. heterochros sp. nov., but is significantly different from it in its smaller body size, relatively shorter antennae, shapes of unguis and mucro, and distinct colour pattern. Key to East Asian species of Pogonognathellus 1. Cuticular ground colour pale white, head and Th. II dark purple . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . P. heterochros sp. nov. Cuticular ground colour pale or grey, head and Th. II not dark purple . . . . . 2 2. Tenaculum scaled, with eight setae on average . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 Tenaculum unscaled, with one or two setae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 3. Tibiotarsus with up to 6, 8, 10 blunt setae . . . . . . . . . . . . P. longicornis (Müller) Tibiotarsus with 0, 0, 2 blunt setae . . . . . . . . . . . . . . . . . . . . . . . . P. beckeri Börner 4. Basal tooth on mucronal dorsal lamella with a toothlet . . . . . . P. borealis Yosii Basal tooth on mucronal dorsal lamella without toothlet . . . . . . . . . . . . . . . . . . 5 5. Maxillary lamella 5 with long beard-like appendix . . . . P. flavescens (Tullberg) Maxillary lamella 5 without distinct beard-like appendix . . . . . . P. mai sp. nov. Discussion Identification of Pogonognathellus species has been confusable for long time, especially when P. flavescens is involved. Pogonognathellus flavescens was first reported in Europe (Tullberg 1871) and then recorded from North America, Asia and even as an invasive species in the sub-Antarctic (Janion et al. 2009). Folsom (1913) described American “flavescens” and divided it into one typical form and three varieties by the variation of ungual teeth and dental spines. Christiansen (1964) recorded many morphotypes and suggested that American “flavescens” is a complex. Latest research has found that American “flavescens” actually comprises multiple species (Felderhoff et al. 2010). East Asian records of Pogonognathellus were located in Japan (Narumi 1951; Yosii 1954, 1956; Chiba 1968), China (Li 1987) and Korea (Lee and Park 1992), and many of them referred to P. flavescens. The previous description of Chinese “flavescens” and “longicornis” (Li 1987) from Sichuan Province agrees with Yosii (1967) and Fjellberg (2007), but it lacks some important description of characters, such as the beard-like appendix, the tibiotarsal spiny setae and the chaetotaxy; so their taxonomic status is in doubt compared with European P. flavescens and P. longicornis. The “P. flavescens” described from North Korea (Lee and Park 1992) also appears to be another species. The Korean specimen has one large distal dental spine, whereas European ones have


1254 T. Wang et al. two (Folsom 1913; Yosii 1967), but it cannot be determined because Korean description is based on only one specimen. Japanese “flavescens” had been reported by many authors (Chiba 1968) and synonymized with P. beckeri by Yosii (1967). Chiba (1968) redescribed Japanese “flavescens” after Yosii’s description, but his description and figures were more similar to those of P. beckeri and morphotype “2cD” for North American “flavescens” (Christiansen 1964) rather than European flavescens, so it cannot be treated as P. flavescens either. Latest research indicates that all known European and North American species could be classified into three clades: bidentatus clade, longicornis clade and pale/grey clade mainly according to the molecular analysis and the chaetotaxy. East Asian species were not included because of the lack of information (Felderhoff et al. 2010). East Asian Pogonognathellus species appear to be included in the three clades. Both P. heterochros and P. mai fit well with the longicornis clade morphologically. Both have two posterior cephalic macrochaetae and one seta on the corpus of tenaculum with the anterior macrochaetae on Abd. IV absent, but their tibiotarsal spiny setae appear in the form of 0, 0, 2 as in pale/grey clade, just like P. flavescens and P. celsus Christiansen, 1964. All East Asian “flavescens” and “longicornis” mentioned above along with P. beckeri and P. borealis lack the description of various characters, such as beard-like appendix, tergal chaetotaxy and tibiotarsal spiny setae, so cannot be determined at present. The confusion about East Asian Pogonognathellus will not be eliminated unless more material is studied both morphologically and molecularly.

Acknowledgements This study was supported by the National Natural Sciences Foundation of China (31101622) and the National Special Transgenic Project (2008ZX08012-005; 2011ZX08012005). Great thanks should be given to Prof. Chen Jianxiu for providing the laboratory with all facilities, and we are obliged to Mr Li Zhaohui in Nanjing Xiaozhuang University, Mr Ma Yitong in Nantong University and Mr Pan Zhixiang in Taizhou University for their cooperation during the expedition in Changbai Mountain.

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