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Research Article
Protura from Hainan Island, China: new species, checklist and distribution
expand article infoYun Bu§, Yan Xiong|, Yun-Xia Luan§, Wen-Ying Yin§
‡ Shanghai Science & Technology Museum, Shanghai, China
§ Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, China
| Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China
¶ South China Normal University, Guangzhou, China
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Abstract

More than 1500 proturan specimens from Hainan Island are systematically studied. An annotated list of all species of Protura from Hainan Island is provided and their geographical distribution is discussed. The genus Paracondeellum is reported from Hainan Island for the first time, and Paracondeellum paradisum sp. nov. is described. The type species Paracondeellum dukouense (Tang & Yin, 1988) is redescribed based on syntype, and the lectotype and paralectotype are designated. The characters of the genus Paracondeellum are redefined, and the two known species are compared in detail. The Protura fauna of Hainan Island is mainly composed of species from the Oriental region, with 91% of the species belonging to the families Berberentulidae and Eosentomidae.

Keywords

distribution, diversity, Paracondeellum, new species, taxonomy, type specimen

Introduction

Protura is a group of tiny soil-dwelling arthropods with more than 800 described species (Bu et al. 2012, 2017; Galli et al. 2018). The diagnosis, distribution, and key to 76 known genera and seven families of Protura worldwide were recently given by Galli et al. (2018). So far, there are 214 species belonging to 43 genera recorded in China (Bu et al. 2012, 2017; Qian et al. 2018).

Hainan Island is the second largest island of China and is located off the southernmost point of the mainland (18°10'–20°10'N, 108°37'–111°03'E; Fig. 1). The tropical forest landscape on Hainan Island is one of the hotspots for biodiversity in China, with a high floral diversity and over 6000 species of insects recorded (Huang 2002). In recent years, many rare insects, such as belonging to Zoraptera, have been found on Hainan Island (Yin et al. 2015).

Figure 1. 

The sampling localities in Hainan Island. Numbers 1–13 indicate the localities listed in Tables 1, 5.

There are several previous publications on the Protura from Hainan Island. The first study reported 14 species of Eosentomidae from Hainan (Yin 1986). Then, eight species of the genus Kenyentulus (Berberentulidae) were described (Yin 1987). Later, 24 species of Protura were recorded in Hainan Province with Fujientomon dicestum Yin, 1977 and Pseudanisentomon yongxingense Yin, 1988 included (Yin 1999, 2002). In 2004, the Protura from Jianfengling Mountain were investigated again. In 2005, Amphientulus sinensis Xiong, Xie & Yin, 2005 was described and seven new records and three undetermined species were newly added (Xiong 2005; Xiong et al. 2005). One of these undetermined species was subsequently described as Anisentomon hainanense Xiong, Bu & Yin, 2008 (Xiong et al. 2008).

In 2011 and 2017, we investigated the soil fauna of Hainan Island on several occasions and collected many proturan specimens. In the present paper, Protentomidae is recorded for the first time and one new species of genus Paracondeellum Yin, Xie & Zhang, 1994 is identified and described. We checked the syntypes of the type species of Paracondeellum dukouense (Tang & Yin, 1988), designated a lectotype and paralectotype, and redescribed it in detail. In addition, based on more than 1500 proturans collected in Hainan Island from 1984 to 2017, a checklist is presented and the distribution of Protura on Hainan Island is summarized.

Materials and methods

Most of specimens were collected between 1984 and 2004, and more recent specimens were collected during the expeditions in 2011 and 2017. All localities sampled so far are listed in Table 1 and shown in Figure 1. All specimens were extracted by means of the Tullgren funnels from soil and humus samples and preserved in 75% ethanol. They were mounted on slides using Hoyer’s solution and dried in an oven at 50 °C.

Table 1.

The sampling localities of Protura in Hainan Island.

Number Locality Coordinates Altitude (m) Sampling years
1 Ledong County, Jianfengling National Natural Reserve 18°23'– 18°52'N, 108°44'–109°02'E 120–330 1984, 1993, 2003, 2004
2 Wuzhishan City, Wuzhishan National Natural Reserve 18°49'–18°59'N, 109°32'–109°43'E 800–1200 1984, 1985, 2004, 2011
3 Wuzhishan City, Diaoluoshan National Natural Reserve 18°43'–18°58'N, 109°43'–110°03'E 500–1000 1985, 2004
4 Haikou City, Dongzhaigang National Natural Reserve 19°51'–20°01'N, 110°32'–110°37'E 20 2004
5 Haikou City, Crater National Geological Park 19°55'N, 110°12'E 223 2003
6 Tunchang County, Meiling Mountain 19°22'N, 110°04'E 150–230 2003
7 Tunchang County, Limu Mountain 19°17'N, 109°77'E 600–1000 2003
8 Baoting County, Ganshenling Provincial Natural Reserve 18°39'N, 109°66'E 500 2003
9 Changjiang County, Qizi bay 19°21'N, 108°40'E 15 2011
10 Baoting, Qixianling National Forest Park 18°42'N, 109°40'E 150 2017
11 Sanya City, Yalong Bay Tropical Paradise Forest Park 18°15'N, 109°38'E 200 2017
12 Sanya City, Luhuitou Park 18°13'N, 109°29'E 80 2017
13 Sanya City, Sanya bay 18°17'N, 109°22'E 5 2017

Observations were made with a phase contrast microscope (Leica DM 2500). Photos were taken by a digital camera (Leica DMC 4500). Line drawings were made using a drawing tube. All specimens are deposited in the collections of Shanghai Natural History Museum (SNHM) and Shanghai Entomological Museum (SEM), Shanghai, China.

Abbreviations used in the text follow the paper by Bu and Yin (2007). Head setae and pores are named according to Rusek et al. (2012) and Shrubovych (2014). The arrangement of the taxa follows the system proposed by Yin (1999).

Results

Taxonomy

Family Protentomidae Ewing, 1936

Paracondeellum Yin, Xie & Zhang, 1994

Diagnosis

Habitus short and robust. Pseudoculi circular without lever. Calyx of maxillary glands globular and smooth. Foretarsal sensilla of the exterior side reduced; interior sensilla b’ absent. Abdominal appendages I–II two-segmented each with four setae, III uni-segmented with two setae. Tergites II–VII without or with few anterior setae. Sternites II–III each with three posterior setae. Sternites IV–VII each with nine posterior setae; sternite VIII with four setae in one row. Female squama genitalis short, with pointed acrostyli (Yin 1999; Galli et al. 2018).

Distribution

South China (Sichuan, Yunnan, Hainan).

Remarks

Paracondeellum Yin, Xie & Zhang, 1994 was originally separated from the genus Condeellum Tuxen, 1963. They have similar shapes of pseudocellus and maxillary gland, and the presence of setae Pc on sternites IV–V, but they can be easily separated by the chaetotaxy of tergite I (seta P5 absent in Paracondeellum but present in Condeellum) and sternite VIII (four setae in Paracondeellum vs six setae in Condeellum). In addition, Paracondeellum can be distinguished from the genus Neocondeellum Tuxen & Yin, 1982 by the shape of pseudocellus (posterior lever absent in Paracondeellum but present in Neocondeellum) and the chaetotaxy of sternites IV–V (setae Pc present in Paracondeellum but absent in Neocondeellum).

Paracondeellum paradisum Bu & Yin, sp. nov.

Figures 2, 3, 4; Tables 2, 4

Diagnosis

Paracondeellum paradisum sp. nov. is characterized by two pairs of A-setae on tergite I, one pair of A-setae, and eight pairs of P-setae on tergites II–VI, absence of A-setae and P2a seta on tergite VII, tergites IX and X with 12 and 10 setae, respectively, absence of seta d4 on dorsal side of head, and female squama genitalis short, with conical acrostylus.

Material examined

Holotype, female (slide no. HN-SY-P2017016) (SNHM), China, Hainan, Sanya City, Yalong Bay Tropical Paradise Forest Park, soil of the tropical rain forest, 200 m elev., 18.25°N, 109.63°E, 22-III-2017, Y. Bu collector. Paratypes, 1 female (slide no. HN-SY-P2017071) (SNHM), same data as holotype.

Description

Holotype: body length 570 μm, yellow-brown, foretarsus darker (Fig. 4A).

Head. Elliptic, length 80 μm, width 50 μm (Fig. 2A). Head setae short, rostrum slightly protruded. Setae d6 and sd6 present, d4 and sd4 absent, d6 and d7 length 6 μm and 7 μm respectively. Pores cp and fp present. Pseudoculus oval, without lever, length 8 μm, width 6.5 μm. PR = 10 (Fig. 2B). Canal of maxillary gland short, with globular calyx and short sausage-like posterior dilation. CF = 10 (Figs 2C, 4B). Labial palpus well developed, with four setae and apical tuft, without basal sensillum (Fig. 2D). Maxillary palpus with two subequal seta-like sensilla (Fig. 2E).

Figure 2. 

Paracondeellum paradisum sp. nov., holotype A head, dorsal view (cp = clypeal pore, fp = frontal pore) B pseudoculus C canal of maxillary gland D labial palpus E maxillary palpus F foretarsus, exterior view G foretarsus, interior view H dorsal thorax, right side I tergite I, right side (al = anterolateral pore, psm = posterosubmedial pore) J tergite VI, right side K comb L female quama genitalis. Arrows indicate pores. Scale bars: 10 μm (B, K); 20 μm (A, C–J, L).

Foretarsus. Length 31 μm, claw length 9 μm, TR = 3.4; empodium length 2 μm, EU = 0.22. Dorsal sensilla t-1 and t-2 slender and long, BS = 0.63; t-3 short and spatulate, not reaching base of claw (Fig. 2G). Exterior side with only sensilla a, b and f present; a spatulate, b and f short (Fig. 2F). Interior sensilla a’ and c’ short sward-like, b’ absent. Relative length of sensilla: t-2 > t-1 > c' > t3 > a > a' > (b = f) (Fig. 2F, G). Length of middle tarsus 15 μm; claw length 10 μm. Length of hind tarsus 17 μm; claw length 12 μm.

Thorax. Thoracic chaetotaxy given in Table 2. Setae 1 and 2 on pronotum subequal in length, 6 μm and 7 μm respectively (Fig. 2H); mesonotum with seven pairs of posterior setae, P5a minute; metanotum with six pairs of posterior setae, P5a absent; setae P1, P1a, P2 on mesonotum 6 μm, 1 μm, 7 μm, respectively; P1a on meso- and metanotum short, pin-shaped (Fig. 2H). Prosternum without seta A2. All setae on thoracic sternites of normal shape. Pores on thorax not observed.

Table 2.

Adult chaetotaxy of Paracondeellum paradisum sp. nov.

Segment Dorsal Ventral
Formula Setae Formula Setae
Th. I 4 1, 2 (2+2)/6 A1, M
P1, 2, 3
II 6/14 A2, 4, M (4+2)/4 A1, 2, M
P1, 1a, 2, 3, 4, 5, 5a P1, 2
III 6/12 A2, 4, M (6+2)/4 A1, 2, 3, M
P1, 1a, 2, 3, 4, 5 P1, 2
Abd. I 4/12 A1, 5 4/2 A1, 2
P1, 1a, 2, 2a, 3, 4 P1
II–III 2/16 A1 4/3 A1, 2
P1, 1a, 2, 2a, 3, 4, 4a, 5 Pc, 2
IV–VI 2/16 A1 4/9 A1, 2
P1, 1a, 2, 2a, 3, 4, 4a, 5 Pc, 1, 1a, 2, 3
VII 0/16 4/9 A1, 2
P1, 1a, 2, 3, 3a, 4, 4a, 5 Pc, 1, 1a, 2, 3
VIII 4/14 A1, 3
P1, 1a, 2, 2a, 3, 3a, 4 4 1, 2
IX 12 1, 1a, 2, 2a, 3, 4 4 1, 2
X 10 1, 2, 2a, 3, 4 4 1, 2
XI 6 6 1, 2, 3
XII 9 6

Abdomen. Abdominal chaetotaxy given in Table 2. Tergite I with two pairs of anterior setae (A1, A5) and six pairs of posterior setae, A5 short, sensillum-shaped (Fig. 2I). Tergites II–VI with one pair of anterior (A1) and eight pairs of posterior setae, P2a present and P3a absent (Figs 2J, 3A, 4E, F). Tergite VII without anterior setae and with eight posterior setae, P2a absent and P3a present (Figs 3B, C, 4E, F). Accessory setae P1a on tergites I–V short pin-shaped (4 μm), on tergites VI–VII normal (5 μm). Accessory setae P2a and P4a always pin-shaped, 2 μm in length. P3a on tergite VII of normal shape and 5 μm long (Fig. 4E, F). Tergite VIII with two pairs of anterior setae (A1, A3) (Fig. 4C). Posterior central seta Pc present on sternites IV–VII, sensillum shaped, 4–5 μm long (Figs 3A, C, 4F). P1a on sternites IV–VI short, pin-shaped (Fig. 3A), on sternite VII setiform (Fig. 3C).

Figure 3. 

A–C Paracondeellum paradisum sp. nov., holotype A sternite VI (spm = sternal posteromedial pore) B tergite VII, right side C sternite VII (spsm = sternal posterosubmedial pore). D–E Paracondeellum dukouense (Tang & Yin, 1988) holotype D foretarsus, exterior view E foretarsus, interior view. Arrows indicate pores. Scale bars: 20 μm.

Figure 4. 

Paracondeellum paradisum sp. nov., holotype A habitus B canal of maxillary gland C tergites VIII–XII D sternites VIII–XII E tergites V–VII F sternites VI–VII. Scale bars: 100 μm (A); 20 μm (B–F).

Tergites I–VII with pores psm and al (Fig. 2I, J), VIII with pores psm only, IX–XI without pores, XII single median pore. Sternites I–VI each with single posteromedial pore spm (Figs 3A, 4F), VII with three posteromedial pores (Figs 3C, 4F), VIII with single posteromedial pore (Fig. 4D), IX–XI without pores, XII with one pair of anterolateral sal pores.

Abdominal appendages typical of the genus. Subapical setae and apical setae on appendage III 11 μm and 5 μm long respectively. Striate band on abdominal segment VIII reduced to a single serrate line (Fig. 4D). Comb on abdomen VIII rectangular, with 10 teeth, 10 μm wide (Fig. 2K). Female squama genitalis short, with conical acrostylus (Fig. 2L).

Etymology

Latin “paradisum”, after “Paradise Forest Park” where type specimens were collected.

Distribution

China (Hainan)

Remarks

The genus Paracondeellum Yin, Xie & Zhang, 1994 is endemic to China and was previously known by a single species, P. dukouense, from Sichuan and Yunnan provinces. Paracondeellum paradisum sp. nov. differs from P. dukouense in the shape of foretarsal sensilla, pseudoculus, and female squama genitalis, and in the body chaetotaxy. A comparison of the morphology of these two species is given in Table 4.

Paracondeellum dukouense (Tang & Yin, 1988)

Figures 3, 5; Tables 3, 4

Diagnosis

Paracondeellum dukouense (Tang & Yin, 1988) is characterized by the one pair of A-setae on tergite I, absence of A-setae and P1a seta on tergites II–VI, absence of A-setae and nine pairs of P-setae (P2a present) on tergite VII, tergites IX and X with 14 and 12 setae respectively, absence of seta d4 on head, and female squama genitalis with pointed acrostylus.

Material examined

Lectotype, female (slide no. 1), paralectotype, female (slide no. 2) (SEM), China, Sichuan, Dukou City (currently, Panzhihua City), Jinjiang County, soil under grass, 1155 m elev., 26.55N, 101.85E, 26-IX-1985, B.W. Tang and G.T. Jin collectors. We designated as the lectotype the female on slide no. 1 and the other female on slide no. 2 as the paralectotype.

Redescription

Body length of holotype 880 μm and paratype 720 μm; yellow-brown, with foretarsus darker (Fig. 5A).

Figure 5. 

Paracondeellum dukouense (Tang & Yin, 1988), holotype A habitus B canal of maxillary gland C head, dorsal view D prosternum E mesosternum F tergite VI G tergites VII–VIII H sternite VI I sternite VII J sternite V K tergites VIII–XII L sternites VIII–XII. Arrows indicate pores. Scale bars: 20 μm.

Head. Elliptic, length 93–100 μm, width 70 μm. Dorsal setae longer than subdorsal and lateral ones, rostrum slightly protruded (Fig. 5C). Setae d6 and sd6 present, sd6 sensillum-shaped; d4 and sd4 absent; d6 and d7 11 μm and 6 μm long, respectively (Fig. 5C). Pores cp and fp present. Pseudoculus round, without lever, length 13 μm, width 11 μm. PR = 7.2–7.7 (Fig. 5C). Canal of maxillary gland short, with globular calyx and sausage-like posterior dilation. CF = 13.3–14.3 (Fig. 5B). Labial palpus well developed, with four setae and apical tuft, without basal sensillum. Maxillary palpus with two subequal sensilla.

Foretarsus. Length 46–50 μm, claw length 15–17 μm, TR=2.9–3.1; empodium length 4–5 μm, EU=0.24–0.33. Dorsal sensilla t-1 and t-2 slender and long, BS=0.66; t-3 short sward-like, nearly reaching base of claw (Fig. 3D). Exterior slide with only sensilla a, b and f present; a spatulate, b and f short sward-like (Fig. 3D). Interior sensilla a’ and c’ short sward-like, b’ absent (Fig. 3E). Relative length of sensilla: t-2 > t-1 > c' > a > t3 > a' > (b = f) (Fig. 3D, E). Length of middle tarsus 20 μm; claw length 12 μm. Length of hind tarsus 23 μm; claw length 15 μm.

Thorax. Thoracic chaetotaxy given in Table 3. Setae 1 and 2 on pronotum subequal in length, 10 μm long; mesonotum with seven pairs of posterior setae, P5a minute; metanotum with six pairs of posterior setae, P5a absent; setae P1, P1a, P2 on mesonotum 10 μm, 1.5 μm, 14 μm respectively; P1a on meso- and metanotum short, pin-shaped. Prosternum with anterior seta A2 (Fig. 5D), meso- and metasternum each with four posterior setae (Fig. 5E), metasternum with six anterior setae. All setae on sterna normal. Pores on thorax not detectable.

Table 3.

Adult chaetotaxy of Paracondeellum dukouense (Tang & Yin, 1988).

Segment Dorsal Ventral
Formula Setae Formula Setae
Th. I 4 1, 2 (4+2)/6 A1, 2, M
P1, 2, 3
II 6/14 A2, 4, M (4+2)/4 A1, 2, M
P1, 1a, 2, 3, 4, 5, 5a P1, 2
III 6/12 A2, 4, M (6+2)/4 A1, 2, 3, M
P1, 1a, 2, 3, 4, 5 P1, 2
Abd. I 2/12 A5 4/2 A1, 2
P1, 1a, 2, 2a, 3, 4 P1
II–III 0/14 4/3 A1, 2
P1, 2, 2a, 3, 4, 4a, 5 Pc, 2
IV–VI 0/14 4/9 A1, 2
P1, 2, 2a, 3, 4, 4a, 5 Pc, 1, 1a, 2, 3
VII 0/18 4/9 A1, 2
P1, 1a, 2, 2a, 3, 3a, 4, 4a, 5 Pc, 1, 1a, 2, 3
VIII 6/14 A1, 3, 5
P1, 1a, 2, 2a, 3, 3a, 4 4 1, 2
IX 14 1, 1a, 2, 2a, 3, 3a, 4 4 1, 2
X 12 1, 2, 2a, 3, 3a, 4 4 1, 2
XI 6 6 1, 2, 3
XII 9 6

Abdomen. Abdominal chaetotaxy given in Table 3. Tergite I with one pair of anterior setae (A5) and six pairs of posterior setae, A5 short, sensillum-shaped. Tergites II–VI without anterior setae and seven pairs of posterior setae, P2a present, P1a and P3a absent (Fig. 5F). Tergite VII without anterior setae and with nine pairs of posterior setae, both P2a and P3a present (Fig. 5G). Accessory setae P2a and P4a on tergites II–VII short, sensillum-shaped, 4 μm in length, P1a and P3a on tergites VII normal, 9–10 μm in length (Fig. 5F, G). Tergite VIII with three pairs of anterior setae (A1, A3, A5) and seven pairs of posterior setae, P3a short (5 μm) (Fig. 5G, K, L). Posterior central seta Pc present on sternites IV–VII slender, 8–9 μm long (Fig. 5H–J). P1a on sternites IV–VI short pin-shaped, 2 μm long (Fig. 5H, J), on sternite VII as normal seta, 9 μm long (Fig. 5I). Sternites IX and X with short P3a seta (Fig. 5L), which had been omitted in original description.

Tergites I–VII with pores psm and al, VIII with pores psm only, IX–XI without pores, XII with single median pore. Pores on sternites I–VI not observed due to the opacity of the old specimens (Fig. 5H, J); three posteromedial pores observed on sternite VII (Fig. 5I), VIII with posteromedial pore (Fig. 5L), IX–XI without pores, XII with one pair of sal pore.

Abdominal appendages typical of the genus. Subapical setae and apical setae on appendage III 12–13 μm and 6–8 μm long, respectively. Striate band on abdominal segment VIII reduced to a single serrate line (Fig. 5G, K, L). Comb on abdomen VIII rectangular, with 10 teeth, 12–13 μm wide (Fig. 5K). Female squama genitalis short, with pointed acrostylus.

Etymology

Named for Dukou City (now Panzhihua City, Sichuan Province) where type specimens were collected.

Distribution

China (Sichuan, Yunnan).

Remarks

Paracondeellum dukouense was originally described based on two syntypes (Tang and Yin 1988). In the original description (Tang and Yin 1988) and in the monograph of Yin (1999), most important characters such as foretarsal sensilla, pseudoculus, maxillary gland, as well as body chaetotaxy were briefly described and illustrated. After careful study of type specimens under a modern phase contrast microscope with higher resolution, we find that sensillum c’ is present on the foretarsus and that some of the setae on the body were previously ignored due to the lower resolution of the microscope used. We correct here these mistakes in the original description and supplement the description of head chaetotaxy, the porotaxy, and the shapes of setae on the body. Table 4 compares P. dukouense with the new species.

Table 4.

Comparison between Paracondeellum paradisum sp. nov. and P. dukouense (Tang & Yin, 1988).

Paracondeellum paradisum sp. nov. P. dukouense
body length (μm) 570 720–880
pseudoculus (μm) 8 13
foretarsus (μm) 31 46–50
sensilla b and f short, rod-like longer, sward-like
sensillum t-3 short and spatulate longer, sward-like
A-setae on tergite I 4 (A1, A5) 2 (A5)
A-setae on tergites II–VI 2 (A1) 0
P-setae on tergites II–VI 16 (P1a present) 14 (P1a absent)
P-setae on tergite VII 16 (P2a absent) 18 (P2a present)
A-setae on tergite VIII 4 (A1, A3) 6 (A1, A3, A5)
setae on tergite IX 12 (P3a absent) 14 (P3a present)
setae on tergite X 10 (P3a absent) 12 (P3a present)
A-setae on prosternum 2 (A2 absent) 4 (A2 present)

List of species from Hainan Island

Family Protentomidae Ewing, 1936

Paracondeellum paradisum sp. nov.

Description

The description is given above.

Family Berberentulidae Yin, 1983

Baculentulus tienmushanensis (Yin, 1963)

Material examined

1 male, 1 mj, locality 3, 19-I-1985, coll. G. T. Jin & Z. Y. Liu. 4 females, 1 mj, locality 5, 26-II-2003; 1 female, locality 1, 14-I-2004; 10 females, 6 mj, locality 2, 27-I-2004, coll. Y. Xiong. 1 mj, locality 11, 22-III-2017, coll. Y. Bu.

Distribution

Widely distributed in China (Hainan, Zhejiang, Shanghai, Jiangxi, Anhui, Hubei, Sichuan, Chongqing, Guizhou, Yunnan, Ningxia, Gansu, Shaanxi, Henan, Hebei, Liaoning, Neimenggu).

Kenyentulus ciliciocalyci Yin, 1987

Material examined

5 females, locality 1, 27-XI-1984, coll. G. T. Jin & Z. Y. Liu. 1 female, VI-1993; 1 female, IV-1994, locality 1, coll. C. H. Liao. 9 females, 2 males, locality 5, 26-II-2003; 1 female, locality 6, 2-III-2003; 1 female, locality 5, 15-VI-2003; 6 females, 1 male, locality 1, 6-X-2003; 9 females, 2 males, 13 mj, locality 1, 14-I-2004; 7 females, 3 males, locality 1, 15-I-2004; 1 female, locality 1, 14-IV-2004; 2 females, 5 males, 1 mj, locality 1, 15-VII-2004, coll. Y. Xiong. 2 females, 1 male, 2 mj, locality 9, 20-III-2011, coll. Y. Bu & C. W. Huang. 14 females, 10 male, 1 mj, locality 11, 22-III-2017; 3 males, locality 12, 17-X-2017, coll. Y. Bu.

Distribution

Widely distributed in China (Hainan, Zhejiang, Hunan, Sichuan, Chongqing, Guizhou, Yunnan, Shaanxi).

Kenyentulus dolichadeni Yin, 1987

Material examined

3 females, locality 2, 14-XI-1984, coll. G. T. Jin & Z. Y. Liu.

Distribution

China (Hainan, Zhejiang, Guangxi, Guizhou, Hubei, Sichuan, Jiangxi).

Kenyentulus hainanensis Yin, 1987

Material examined

4 females, 1 male, locality 1, 30-XI-1984; 2 females, 2 males, locality 2, 14-XI-1984; 1 male, 2 mj, locality 3, 19-I-1985, coll. G. T. Jin & Z. Y. Liu.

Distribution

China (Hainan, Guangdong).

Kenyentulus henanensis Yin, 1983

Material examined

2 female, 1 male, locality 2, 19-XI-1984, coll. G. T. Jin & Z. Y. Liu.

Distribution

Widely distributed in China (Hainan, Zhejiang, Jiangxi, Henan, Hubei, Guizhou, Yunnan, Ningxia).

Kenyentulus japonicus (Imadate, 1961)

Material examined

2 females, locality 2, 14-XI-1984; 5 females, 5 males, locality 1, 25-XI-1984, coll. G. T. Jin & Z. Y. Liu.

Distribution

Widely distributed in China (Hainan, Zhejiang, Jiangsu, Shanghai, Jiangxi, Anhui, Hunan, Sichuan, Guizhou, Yunnan, Shaanxi); Japan.

Kenyentulus jianfengensis Yin, 1987

Material examined

4 females, locality 1, 1-XII-1984, coll. G. T. Jin & Z. Y. Liu. 2 females, 1 male, 1 mj, locality 1, 6-X-2003; 7 females, 5 males, 2 mj, locality 1, 15-I-2004; 1 mj, locality 3, 27-I-2004; 3 females, 1 males, 1 mj, locality 1, 14-IV-2004; 7 females, 9 males, locality 1, 15-VII-2004, coll. Y. Xiong.

Distribution

China (Hainan, Guizhou).

Kenyentulus jinghongensis Yin, 1983

Material examined

3 females, locality 1, 25-XI-1984, coll. G. T. Jin & Z. Y. Liu.

Distribution

China (Hainan, Yunnan, Guizhou).

Kenyentulus minys Yin, 1983

Material examined

2 females, 2 males, locality 1, 19-XI-1984, coll. G. T. Jin & Z. Y. Liu.

Distribution

China (Hainan, Yunnan, Guangxi, Jiangxi)

Amphientulus sinensis Xiong, Xie & Yin, 2005

Material examined

1 female, locality 1, 17-XII-2002; 1 female, locality 2; 8 females, 4 males, 1 mj, locality 3, 27-I-2004, coll. Y. Xiong.

Distribution

China (Hainan, Guangdong).

Family Sinentomidae Yin, 1965

Sinentomon erythranum Yin, 1965

Material examined

1 female, 1male, 1 mj, locality 5, 26-II-2003; 1 mj, locality 1, 6-X-2003; 7 females, locality 1, 15-VII-2004, coll. Y. Xiong. 1 female, 1 LI, locality 13, 16-X-2017; 1 LI, locality 12, 17-X-2017, coll. Y. Bu.

Distribution

Widely distributed in South China (Hainan, Shanghai, Jiangsu, Zhejiang, Anhui, Fujian, Guangxi, Guangdong, Hunan, Guizhou, Yunnan).

Fujientomidae Yin, 1996

Fujientomon dicestum Yin, 1977

Material examined

1 female, locality 5, 26-II-2003, coll. Y. Xiong.

Distribution

China (Hainan, Shanghai, Jiangsu, Zhejiang, Anhui, Ningxia).

Eosentomidae Berlese, 1909

Eosentomon actitum Zhang, 1983

Material examined

8 females, 6 males, 2 mj, locality 1, XII-1984; 24 females, 24 males, 27 mj, locality 3, 23-I-1985, coll. G. T. Jin & Z. Y. Liu. 2 females, 3 males, locality 8, 22-II-2003, coll. Y. Xiong. 2 females, 3 mj, locality 11, 22-III-2017, coll. Y. Bu.

Distribution

China (Hainan, Guangdong, Sichuan).

Eosentomon hainanense Yin, 1986

Material examined

40 females, 33 males, 2 mj, locality 1, 25-XI-1984, coll. G. T. Jin & Z. Y. Liu. 2 females, VI-1993, locality 1, coll. C. H. Liao. 1 female, 5 males, locality 8, 22-II-2003; 4 females, 1 male, locality 6, 2-III-2003; 1 female, 3 males, 4 mj, locality 5, 15-VI-2003; 19 female, 15 males, 8 mj, locality 1, 7-X-2003; 33 females, 31 males, 15 mj, locality 1, 14-I-2004; 1 male, locality 3, 960 m elev., 27-I-2004; 8 females, 8 males, 1 mj, locality 1, 15-VII-2004, coll. Y. Xiong.

Distribution

China (Hainan, Yunnan).

Eosentomon iban Imadate, 1965

Material examined

2 females, 2 males, locality 1, 27-XI-1984, coll. G. T. Jin & Z. Y. Liu.

Distribution

China (Hainan); Malaysia, Brunei.

Eosentomon jinhongense Yin, 1982

Material examined

2 females, 1 male, locality 2, 14-XI-1984, coll. G. T. Jin & Z. Y. Liu.

Distribution

China (Hainan, Yunnan).

Eosentomon margarops Yin & Zhang, 1982

Material examined

1 female, 2 males, 1 mj, locality 5, 26-II-2003; 1 female, 1 male, 2 mj, locality 5, 15-VI-2003; 1 female, 2 males, locality 1, 6-X-2003; 6 females, 3 males, 1 mj, locality 1, 15-I-2004; 2 females, 1 male, 1 mj, locality 2, 820 m elev., 27-I-2004; 3 females, 2 males, 2 mj, locality 3, 1000 m elev., 27-I-2004; 2 females, 1 male, locality 1, 14-IV-2004; 2 females, locality 1, 15-VII-2004, coll. Y. Xiong. 1 female, locality 10, 23-III-2017, coll. Y. Bu.

Distribution

China (Hainan, Guangdong, Sichuan).

Eosentomon novemchaetum Yin, 1965

Material examined

1 female, locality 11, 22-III-2017, coll. Y. Bu.

Distribution

China (Hainan, Shanghai, Jiangsu, Anhui, Jiangxi, Liaoning, Shaanxi)

Eosentomon orientale Yin, 1965

Material examined

1 female, locality 1, 25-XI-1984, coll. G. T. Jin & Z. Y. Liu.

Distribution

Widely distributed in China (Hainan, Shanghai, Jiangsu, Zhejiang, Anhui, Jiangxi, Hubei, Hunan, Guangxi, Guangdong, Sichuan, Chongqing, Guizhou, Ningxia, Shaanxi, Liaoning).

Eosentomon sakura Imadate & Yosii, 1959

Material examined

5 females, 3 males, locality 1, 25-XI-1984, coll. G. T. Jin & Z. Y. Liu. 13 females, 7 males, 9 mj, locality 8, 22-II-2003; 1 female, 1 mj, locality 5, 20-I-2003; 8 females, 13 males, 7 mj, locality 5, 26-II-2003; 1 female, 1 male, locality 6, 2-III-2003; 2 females, 5 males, 2 mj, locality 5, 15-VI-2003; 2 females, 1 mj, locality 1, 6-X-2003; 3 females, 1 male, 2 mj, locality 7, 13-VII-2003; 5 females, 2 males, 2 mj, locality 1, 15-I-2004; 46 females, 45 males, 29 mj, locality 4, 23-I-2004; 12 females, 20 males, 10 mj, locality 2, 820 m elev., 27-I-2004; 5 females, 5 males, 2 mj, locality 1, 500 m elev., 27-I-2004, coll. Y. Xiong. 1 male, locality 2, 20-III-2011, coll. Y. Bu & C. W. Huang. 8 females, 7 males, 3 mj, locality 11, 22-III-2017, coll. Y. Bu.

Distribution

Widely distributed in China (Hainan, Shanghai, Jiangsu, Zhejiang, Anhui, Jiangxi, Hubei, Hunan, Guangxi, Guangdong, Yunnan, Sichuan, Fujian, Guizhou, Taiwan, Hong Kong, Shaanxi).

Eosentomon shanum (Zhang, 1984)

Material examined

2 females, 1 male, locality 4, 23-I-2004; 1 female, 2 males, locality 1, 14-IV-2004; 5 females, 1 mj, locality 1, 15-VII-2004, coll. Y. Xiong.

Distribution

China (Hainan, Guangxi, Hunan, Jiangxi).

Eosentomon spanum Yin, 1986

Material examined

1 female, 1 male, locality 1, 27-XI-1984, coll. G. T. Jin & Z. Y. Liu.

Distribution

China (Hainan).

Eosentomon tropicum Yin, 1986

Material examined

5 females, locality 1, 25-XI-1984, coll. G. T. Jin & Z. Y. Liu. 1 female, VII-1993, locality 1, coll. C. H. Liao. 1 female, 3 males, 3 mj, locality 8, 22-II-2003; 4 females, 3 males, 4 mj, locality 1, 6-X-2003; 2 mj, locality 1, 15-I-2004; 3 females, 1 male, locality 1, 15-VII-2004, coll. Y. Xiong. 2 females, locality 11, 22-III-2017, coll. Y. Bu.

Distribution

China (Hainan).

Eosentomon xishaense Yin, 1988

Material examined

2 females, locality 1, 27-XI-1984, coll. G. T. Jin & Z. Y. Liu. 1 mj, VI-1993, locality 1, coll. C. H. Liao. 1 female, locality 5, 20-I-2003; 3 mj, locality 1, 14-IV-2004; 4 females, 2 males, locality 1, 15-VII-2004, coll. Y. Xiong. 1 female, locality 9, 20-III-2011, coll. Y. Bu & C. W. Huang. 2 females, 1 male, 1 mj, locality 11, 22-III-2017; 1 male, locality 10, 23-III-2017, coll. Y. Bu.

Distribution

China (Hainan, Xisha Islands, Yongxing Island).

Eosentomon yanshanense Yin & Zhang, 1982

Material examined

2 females, locality 1, 25-XI-1984, coll. G. T. Jin & Z. Y. Liu. 2 females, 4 males, 7 mj, locality 6, 2-III-2003; 9 females, 3 males, 10 mj, locality 4, 23-I-2004; 2 females, 2 males, locality 1, 14-IV-2004; 2 females, 1 mj, locality 1, 15-VII-2004, coll. Y. Xiong.

Distribution

China (Hainan, Guangxi, Guangdong, Fujian, Jiangxi, Hunan, Hubei, Yunnan).

Eosentomon zhanjiangense Zhang, 1983

Material examined

2 females, locality 1, 19-I-1985, coll. G. T. Jin & Z. Y. Liu. 1 females, 2 males, locality 1, 14-IV-2004, coll. Y. Xiong.

Distribution

China (Hainan, Guangdong).

Anisentomon hainanense Xiong, Bu & Yin, 2008

Material examined

1 female, 1 male, locality 1, 6-X-2003, coll. Y. Xiong.

Distribution

China (Hainan).

Anisentomon quadrisetum Zhang & Yin, 1981

Material examined

1 female, 1 male, locality 1, 7-X-2003, 14 females; 7 males, locality 1, 14-I-2004, coll. Y. Xiong. 1 male, 1 mj, locality 11, 22-III-2017, coll. Y. Bu.

Distribution

China (Hainan, Guangxi, Guangdong).

Neanisentomon yuenicum Zhang & Yin, 1984

Material examined

1 female, locality 1, 14-IV-2004, coll. Y. Xiong. 1 female, 1 male, locality 10, 23-III-2017, coll. Y. Bu.

Distribution

China (Hainan, Guangdong).

Paranisentomon tuxeni (Imadate & Yosii, 1959)

Material examined

6 females, 1 mj, locality 3, 1000 m elev., 27-I-2004, coll. Y. Xiong.

Distribution

China (Hainan, Hubei, Hunan, Jiangxi, Anhui, Guizhou, Shaanxi).

Pseudanisentomon paurophthalmum Zhang & Yin, 1984

Material examined

1 female, 1 mj, locality 11, 22-III-2017, coll. Y. Bu.

Distribution

China (Hainan, Guangxi).

Pseudanisentomon molykos Zhang & Yin, 1984

Material examined

5 females, 2 males, 1 mj, locality 1, 6-X-2003; 1 female, locality 1, 14-IV-2004, coll. Y. Xiong.

Distribution

China (Hainan, Guangdong, Guangxi, Yunnan).

Pseudanisentomon sininotiale Zhang & Yin, 1984

Material examined

2 females, locality 1, 27-XI-1984, coll. G. T. Jin & Z. Y. Liu. 2 females, 4 males, locality 4, 23-I-2004; 1 male, locality 3, 600 m elev., 27-I-2004, coll. Y. Xiong.

Distribution

China (Hainan, Guangxi, Hunan).

Discussion

The 34 species of Protura recorded from Hainan Island belong to 11 genera and five families (Protentomidae, Berberentulidae, Sinentomidae, Fujientomidae and Eosentomidae) (Table 5). Most species (91%) belong to Eosentomidae (21 species) and Berberentulidae (10 species), while the other three families are represented by one species each. Both Berberentulidae and Eosentomidae are widely distributed in China and have high species richness. In contrast, Sinentomidae, Protentomidae, and Fujientomidae each has fewer species occurring in China. Undoubtedly, proturans found in Hainan Island are mainly related to the fauna of Oriental Region and are distinctly different from those from Russian Far East and Siberia (Bu et al. 2014; Shrubovych 2014), which are dominated by the family Acerentomidae.

Table 5.

The list of proturan species from Hainan Island and their distribution in Hainan Island and three neighboring mainland provinces.

Classification Species Hainan Guangdong Guangxi Yunnan
Acerentomata Yin, 1996
Protentomidae Ewing, 1936
Paracondeellum Yin, Xie & Zhang, 1994 P. paradisum sp. n.* 11**
Berberentulidae Yin, 1983
Baculentulus Tuxen,1977 B. tienmushanensis (Yin, 1963) 2, 3, 5, 11 +
Kenyentulus Tuxen, 1981 K. ciliciocalyci Yin, 1987 1, 5, 6, 9, 11, 12 +
K. dolichadeni Yin, 1987 2
K. hainanensis Yin, 1987 1, 3 +
K. henanensis Yin, 1983 2 +
K. japonicus (Imadate, 1961) 2 +
K. jianfengensis Yin, 1987 1, 2
K. jinghongensis Yin, 1983 1 +
K. minys Yin, 1983 1 + +
Amphientulus Tuxen, 1981 A. sinensis Xiong, Xie & Yin, 2005 1, 3 +
Sinentomata Yin, 1996
Sinentomidae Yin, 1965
Sinentomon Yin, 1965 S. erythranum Yin, 1965 1, 5, 12, 13 + + +
Fujientomidae Yin, 1996
Fujientomon Yin, 1977 F. dicestum Yin, 1977 5
Eosentomata Yin, 1996
Eosentomidae Berlese, 1909
Eosentomon Berlese, 1909 E. actitum Zhang, 1983 1, 3, 8, 11 +
E. hainanense Yin, 1986* 1, 3, 5, 6, 8 + +
E. iban Imadate, 1965 1
E. jinhongense Yin, 1982 2 +
E. margarops Yin & Zhang, 1982 1, 2, 3, 5, 10 +
E. novemchaetum Yin, 1965 11
E. orientale Yin, 1965 1 + +
E. sakura Imadate & Yosii, 1959 1, 2, 4–8, 11 + + +
E. shanum (Zhang, 1984) 1, 4 +
E. spanum Yin, 1986* 1
E. tropicum Yin, 1986* 1, 8, 11
E. xishaense Yin, 1988 1, 5, 9–11
E. yanshanense Yin & Zhang, 1982 1, 4, 6 + + +
E. zhanjiangense Zhang, 1983 1 +
Anisentomon Yin, 1977 A. hainanense Xiong, Bu & Yin, 2008* 1
A. quadrisetum Zhang & Yin, 1981 1, 11 + +
Neanisentomon Zhang & Yin, 1984 N. yuenicum Zhang & Yin, 1984 1, 10 +
Paranisentomon Zhang & Yin, 1984 P. tuxeni (Imadate & Yosii, 1959) 3
Pseudanisentomon Zhang & Yin, 1984 P. paurophthalmum Zhang & Yin, 1984 11 +
P. molykos Zhang & Yin, 1984 1 + +
P. sininotiale Zhang & Yin, 1984 1, 4 +

By comparing the species distribution, we found that the Protura fauna of Hainan Island is closely related to those of neighboring mainland regions (Yin 1999; Szeptycki 2007), and there are 13, 10, and 11 species shared with Guangdong, Guangxi, and Yunnan provinces, respectively (Fig. 1; Table 5), which is consistent with the geological history of Hainan Island (Wang 1991; Zhang and Fang 2012). Until the Quaternary period (2.5 million years ago), Hainan Island was still connected with Leizhou Peninsula of Guangdong Province. In the Middle Pleistocene, fault depression led to the separation of Hainan Island from the mainland. With sea level fluctuations, Hainan Island was connected to or separated from the mainland for several times. Since the end of the Quaternary period, due to the drastically rise of sea level, Hainan Island has been separated from the mainland without interruption.

Among the mainland regions neighboring Hainan Island, the Protura fauna of Yunnan Province has been systematically studied (Zhang et al. 1996; Yin et al. 2000), and nearly 80 species were reported from that province, with the Berberentulidae and Ensentomidae having fairly high diversity (Zhang et al. 1996; Yin et al. 2000). In this study, we found the diversity of Protura fauna from Hainan Island is very similar to that from Yunnan Province. The only difference is the presence of family Hesperentomidae in Yunnan, which is absent in Hainan Island.

Sampling localities in Hainan Island are still sparse, and additional collection of proturans should be made in the future, so as to reveal the true diversity and provide a better understanding of the biogeography of Protura on the Hainan Island.

Acknowledgements

We give our cordial gratitude to Mr Gentao Jin, Mr Zuyao Liu, Mr Chonghui Liao, Mr Bowei Tang, and Mr Chengwang Huang for their help in the collection of specimens, to Mr Yiming Yang for his help in preparation of slides, to Mr Rongdong Xie for his identification of part specimens and to Dr Yi Bai for his help in preparation of the map of Hainan Island. We also appreciate Professor José G. Palacios-Vargas for his linguistic corrections to the manuscript as well as his valuable advice. Special thanks are given to Dr Julia Shrubovych and Dr Loris Galli for their valuable comments and review of the manuscript. This research was supported by the National Natural Science Foundation of China (no. 31772509, 31471958 and 31772510), the Natural Science Foundation of Shanghai (no. 17ZR1418700), and the Open Project of Shanghai Key Lab for Urban Ecological Processes and Eco-Restoration (no. SHUES2019A11).

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