review of chinese littoral thalassaphorura (collembola: onychiuridae),...

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Review of Chinese littoralThalassaphorura (Collembola:Onychiuridae), with the description oftwo new speciesXin Suna, Yan Gaob & Mikhail B. Potapovc

a Key Laboratory of Wetland Ecology and Environment, NortheastInstitute of Geography and Agroecology, Chinese Academy ofSciences, Changchun, Chinab Institute of Plant Physiology and Ecology, Shanghai Institutesfor Biological Sciences, Chinese Academy of Sciences, Shanghai,Chinac Moscow State Pedagogical University, Moscow, RussiaPublished online: 24 Jan 2014.

To cite this article: Xin Sun, Yan Gao & Mikhail B. Potapov , Journal of Natural History (2014):Review of Chinese littoral Thalassaphorura (Collembola: Onychiuridae), with the description of twonew species, Journal of Natural History, DOI: 10.1080/00222933.2013.839843

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Review of Chinese littoral Thalassaphorura (Collembola: Onychiuridae),with the description of two new species

Xin Suna, Yan Gaob* and Mikhail B. Potapovc

aKey Laboratory of Wetland Ecology and Environment, Northeast Institute of Geography andAgroecology, Chinese Academy of Sciences, Changchun, China; bInstitute of Plant Physiologyand Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences,Shanghai, China; cMoscow State Pedagogical University, Moscow, Russia

(Received 26 August 2012; accepted 1 August 2013)

The present paper is the third contribution to the knowledge of littoral Collembolaof China. Species of the genus Thalassaphorura occurring in sandy and shinglybeaches in China are reviewed. Descriptions of two new species, Thalassaphorurabrevisetosa sp. nov. and Thalassaphorura hainanica sp. nov. are provided.Thalassaphorura duplopunctata and Thalassaphorura lifouensis are recorded forthe first time from China, and T. duplopunctata is re-described mainly based onChinese specimens. Thalassaphorura brevisetosa sp. nov. is characterized by havingstrongly reduced unguiculus and very short body chaetae. Thalassaphorura haina-nica sp. nov. resembles Thalassaphorura pomorskii from which it differs by 2 + 2pso on Abd. IV, absence of chaetae on Th. I sternum and four chaetae on subcoxa1 of leg I, among other characters.

http://www.zoobank.org/urn:lsid:zoobank.org:pub:B8AC3DB3-DF12-47E2-ACEE-969D72C594C8

Keywords: taxonomy; chaetotaxy; Pacific coast; Sensilla; springtail

Introduction

Notwithstanding the expressive name of the genus, only five littoral species among 43known species of the genus Thalassaphorura Bagnall, 1949, are known from acrossthe world: Thalassaphorura debilis (Moniez, 1890) from France, Norway andDenmark (Fjellberg 1998), Thalassaphorura duplopunctata (Strenzke 1954) fromGermany, Norway, Iceland and the Arctic islands (Fjellberg 1998),Thalassaphorura hoguei (Palacios-Vargas and Díaz 1995) from Mexico,Thalassaphorura lifouensis (Thibaud and Weiner 1997) from New Caledonia, andThalassaphorura thalassophila (Bagnall 1937) from Scotland and France. To date,neither the genus Thalassaphorura, nor any other member of the family Onychiuridaewas recorded in seashore habitats in China.

During the course of our investigation of the littoral Collembola of China(Potapov et al. 2011; Bu et al. 2012), some species belonging to the familyOnychiuridae (mainly Thalassaphorura) were found as a very abundant componentin supralittoral communities. In the present paper, two species new to science, namelyThalassaphorura brevisetosa sp. nov. and Thalassaphorura hainanica sp. nov., aredescribed.

*Corresponding author. Email: [email protected]

Journal of Natural History, 2013http://dx.doi.org/10.1080/00222933.2013.839843

© 2013 Taylor & Francis

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Material and methods

All specimens were collected by simple flotation methods using salt water andmounted on slides with Hoyer’s solution after clearing in lactic acid. The slideswere dried in an oven at 60°C and were studied using a Nikon Eclipse 80i microscope.Material is deposited in the Shanghai Institute of Plant Physiology and Ecology,Chinese Academy of Sciences, Shanghai (SIPPE, China), Northeast Instituteof Geography and Agroecology, Chinese Academy of Sciences, Changchun(NEIGAE, China) and Moscow State Pedagogical University (MSPU, Russia).

Abbreviations used in descriptions

Labial types are named after Fjellberg (1999). The chaetal nomenclature of labiumareas follows Massoud (1967) and D’Haese (2003). Chaetae on anal valves are namedafter Yoshii (1996), furcal area after Pomorski (1996) and Weiner (1996).

Ant., antennal segments; PAO, postantennal organ; Th., thoracic segments; Abd.,abdominal segments; p-chaeta, chaeta of row p; Sp, posterior s-chaeta (e.g. on Abd.V or on head); ms, microsensillum; pso, pseudocellus; AS, anal spines; x, axialpseudopore of Abd. IV.

Taxonomy

Family ONYCHIURIDAE Börner, 1913Genus Thalassaphorura Bagnall, 1949Thalassaphorura brevisetosa sp. nov.

(Figures 1 and 2)

Type material

Holotype: male, Yangma Island, 37°27′N, 121°36′E, sandy beach (No. 81), 22April 2011. Paratypes: 11 females and 9 males, same as holotype; 19 females,37°27′N, 121°30′E, sandy beach (No. 94–101), 23 April 2011. All from ShandongProvince, northeast China, leg. M.B. Potapov, Y.X. Luan and C.W. Huang.Holotype and 20 paratypes (16 females and 4 males) are deposited in SIPPE, 9paratypes (8 female and 1 male) in MSPU, and 10 paratypes (6 females and 4males) in NEIGAE.

Description

Body white in alcohol. Size 750–870 µm in females, 650–800 µm in males; holotype:750 µm. Body subcylindrical, body sides almost parallel.

Pseudocellar formula: 32/133/33343 dorsally, 11/000/00010 ventrally (Figures 1A,B, 2A, E), subcoxa 1 of legs I–III with 1, 1 and 1 pso, respectively. Parapseudocelliabsent. Pseudopore formula: 00/011/11110 dorsally, 00/111/000x0 ventrally.

S-chaetae subcylindrical, well differentiated, formula: 11/011/221121 dorsally,11/000/000100 ventrally (Figures 1A,B, 2A, E). Sp present on dorsal side of head.Tiny and blunt ms, present on Th. II–III.

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Figure 1. Thalassaphorura brevisetosa sp. nov. (A) Dorsal chaetotaxy of head and Th. I–II; (B)dorsal chaetotaxy of Th. III–Abd. VI; (C) organ of Ant. III; (D) labial palp; (E) tibiotarsus III;(F) antenna. Scale bars: 100 µm (A, B, F), 10 µm (C–E).

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Figure 2. Thalassaphorura brevisetosa sp. nov. (A) Ventral side of head; (B) anal valves; (C)maxilla; (D) claw; (E) leg III; (F) ventral side of Abd. II–VI. Scale bars: 100 µm (A, C, E),10 µm (B, D).

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Head. Antennae short and distinctly segmented, as long as head or slightly longer.Length ratio of Ant. I : II : III : IV as about 1 : 1.8 : 1.8 : 2. Ant. IV with subapicalorganite with apex globular; basolateral ms at about one-third length from base. Ant.III sensory organ composed of five papillae, five guard chaetae, two small sensoryrods and two smooth subequal clubs, and a lateral ms (Figure 1C, F). Ant. II with 12chaetae. Ant. I with eight chaetae. Antennal base without distinct granulation. PAOcomposed 16–20 simple vesicles. Dorsal cephalic chaeta d0 present, 3 + 3 p-chaetaepresent between two inner posterior pso, p1 anterior to others (Figure 1A). Mandiblewith strong molar plate and four apical teeth. Maxilla bearing three teeth and sixlamellae (Figure 2C). Maxillary outer lobe with a simple palp, one basal chaeta andtwo sublobal hairs. Labral chaetae formula 4/142. Labium with six proximal, fourbasomedian (E, F, G, F) and five basolateral (b, c, d, e, e’) chaetae; labial typeA, papillae A–E respectively with 1, 4, 0, 3 and 2 guard chaetae (Figure 1D).Postlabial chaetae 3 + 3 along ventral groove (Figure 2A).

Body chaetotaxy (Figures 1A, B, and 2F). Ordinary chaetae short, weaklydifferentiated to mesochaetae and macrochaetae, ratio sp : m1 : p1 on Abd. Vtergum = 1 : 0.6 : 1.2. Th. I tergum with 5 + 5 dorsal chaetae. Th. II–III terga with4 + 4 chaetae and Abd. I–III terga with 3 + 3 chaetae respectively on both sides ofaxial line, sometimes with asymmetric chaetae. Abd. IV tergum with asymmetricchaetae, Abd. V tergum without axial chaetae, Abd. VI tergum with one axial chaeta(a0) (Figure 1 B). Th. I, II and III sterna each with 1 + 1 chaetae.

Appendages. Subcoxa 1 of legs I–III with 3, 3 and 3(4) chaetae, subcoxa 2 with 1,3 and 3 chaetae respectively (Figure 2E). Tibiotarsi of legs I, II and III with 18 (1,8, 9) chaetae each. Unguis without teeth. Unguiculus reduced to small blunt process(Figure 1E). Pretarsus armed with transversal circular ridge with two pairs of wartsanterior and lateral (Figures 1E and 2D). Ventral tube with 10 + 10 chaetae: 1 + 1anterior, 7 + 7 distal chaetae, and 2 + 2 basal chaetae. Furca reduced to a field of finegranulation and with four small dental chaetae arranged in two rows below; with onlyone manubrial row of chaetae (Figure 2F).

Genital plate with 8–10 chaetae in females, 24–26 chaetae in males. Male organabsent. Anal valves with numerous acuminate chaetae; each lateral valve with a0 and2a1; upper valves with chaetae a0, 2b1, 2b2, c0, 2c1, 2c2 (Figure 2B). Anal spines seton indistinct papillae, 0.7 times as long as inner edge of hind unguis.

Ecology

Highly abundant in one sample in sand dunes.

Etymology

Named after the short chaetae on the body.

Remarks

The new species is peculiar in its wart-like blunt unguiculus, which was not previouslyfound in the genus. Otherwise, T. brevisetosa sp. nov. resembles two seaside Europeanspecies namely T. debilis and T. thalassophila. The latter is considered to be asynonym of the former (Fjellberg 1998), however, the relationships between these


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two species and all other forms of T. debilis remain unresolved (Sun et al. 2010).Thalassaphorura brevisetosa sp. nov. and T. debilis/thalassophila share pso formula32/133/33343, 1/1/1 pso on subcoxae, 1 + 1/1 + 1/1 + 1 ventral chaetae on Th. I–III,1 + 1/7 + 7/2 + 2 chaetae on ventral tube, and middle-sized anal spines (ratio of AS/hind unguis about 0.7). The new species differs by body being half the size, thepresence of a pair of ventral pso on the abdomen, almost totally reduced unguiculusand shorter chaetae on the body.

Thalassaphorura hainanica sp. nov.(Figures 3 and 4)

Type material

Holotype: female, Qizi Bay, 19°21′N, 108°40′E, sand beach (No. 31), vicinity ofChanghua town, Changjiang County, Hainan Province (western coast), SouthChina, 6April 2011, leg. Y. Bu, C.W. Huang, M.B. Potapov and N.A. Kuznetsova.Paratypes: 6 females and 5 males, same as holotype. Holotype and 5 paratypes (3females and 2 males) are deposited in SIPPE, 2 paratypes (1 female and 1 male) inMSPU, and 4 paratypes (2 females and 2 males) in NEIGAE.

Description

Body white in alcohol. Size 750–800 µm in females, 550–700 µm in males; holotype:800 µm. Body subcylindrical, body sides almost parallel.

Pseudocellar formula: 32/233/33343 dorsally, and 11/000/01120 ventrally (Figures3C–E and 4A), subcoxa 1 of legs I–III each with 2 pso respectively. Parapseudocelliabsent. Pseudopore formula: 00/011/11110 dorsally, 00/111/000x0 ventrally.

S-chaetae cylindrical, well differentiated, formula: 11/011/222121 dorsally, 11/000/000100 ventrally. Sp present on dorsal side of head. Tiny and blunt ms, present onTh. II–III.

Head. Antennae short and distinctly segmented, as long as head. Length ratio ofAnt. I : II : III : IV as about 1 : 1.5 : 1.5 : 2. Ant. IV with subapical organite with apexglobular; basolateral ms at about two-fifths length from base. Ant. III sensory organcomposed of five papillae, five guard chaetae, two small sensory rods and two smoothsubequal clubs, and a lateral ms (Figures 3B and 4B). Ant. II with 13 chaetae. Ant. Iwith eight chaetae. Antennal base with distinct granulation. PAO composed 16–17simple vesicles. Dorsal cephalic chaeta d0 present. 3 + 3 p-chaetae present betweentwo inner posterior pso, p1 anterior to others (Figure 3C). Mandible with strongmolar plate and four apical teeth. Maxilla bearing three teeth and six lamellae.Maxillary outer lobe with a simple palp, one basal chaeta and two sublobal hairs.Labral chaetae formula 4/142. Labium with six proximal, four basomedian (E, F, G,f) and six basolateral (a, b, c, d, e, e’) chaetae; labial type AC, papillae A–Erespectively with 1, 4, 0, 3 and 2 guard chaetae (Figure 3A). Postlabial chaetae4 + 4 along ventral groove (Figure 4A).

Body chaetotaxy (Figure 3C–E). Ordinary chaetae differentiated in mesochaetaeand macrochaetae, ratio sp: m1: p1 on Abd. V tergum = 1 : 0.5 : 1.8. Th. I tergumwith 5 + 5 chaetae. Th. II–III and Abd. I–III terga with 3 + 3 chaetae respectively on

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Figure 3. Thalassaphorura hainanica sp. nov. (A) Labial palp; (B) organ of Ant. III; (C) dorsalchaetotaxy of head and Th. I–II; (D) dorsal chaetotaxy of Th. III–Abd. VI; (E) ventral side ofAbd. II–VI. Scale bars: 100 µm (C–E), 10 µm (A, B).


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Figure 4. Thalassaphorura hainanica sp. nov. (A) Ventral side of head; (B) antenna; (C) analvalves; (D) leg III; (E) tibiotarsus III; (F) furcal area. Scale bars: 100 µm (A, B, D), 10 µm (C, E).

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both side of axial line, without axial chaeta. Abd. IV tergum with one axial chaeta(m0), Abd. V tergum with one axial chaeta (a0), Abd. VI tergum with one axialchaeta (a0) (Figure 3D). Th. I, II and III sterna with 0 + 0, 1 + 1, 1 + 1 chaetae,respectively.

Appendages. Subcoxa 1 of legs I–III with 4, 4 and 4 chaetae, subcoxa 2 with 1, 4and 4 chaetae respectively. Tibiotarsi of legs I, II and III with 18 (1, 8, 9) chaetaeeach. Unguis without teeth. Unguiculus 0.7 times as long as inner edge of unguis,with very narrow inner basal lamella (Figure 4D, E). Ventral tube with 1 + 1 anteriorchaetae, 6 + 6 distal chaetae, 2 + 2 basal chaetae. Furca reduced to a field of finegranulation and with four small dental chaetae arranged in two rows below; only onemanubrial row of chaetae present (Figure 4F).

Genital plate with 11–12 chaetae in females, 20–22 chaetae in males. Male organabsent. Anal valves with numerous acuminate chaetae; each lateral valve with a0 and2a1; upper valves with chaetae a0, 2b1, 2b2, c0, 2c1, 2c2 (Figure 4C). Anal spines seton indistinct papillae, 0.3 times as long as inner edge of hind unguis.

Ecology

The species was collected from the sand covered by scattered vegetation on the outersection of a dune on an oceanic beach.

Etymology

To date the species has only been recorded from Hainan Island.

Remarks

The new species shows the most common pseudocellar formula (32/233/33343) knownamong the species of the genus (Sun et al. 2010). It mostly resembles T. pomorskii Sunet al., 2010 described from forest litter of the Guangxi Province. They share the samepso and s-chaetae dorsal formulae, 5 + 5 dorsal chaetae on Th. I, presence of axialchaeta a0 on Abd. VI tergum, 1 + 1/6 + 6/2 + 2 chaetae on ventral tube, and smallanal spines. T. hainanica sp. nov. differs from T. pomorskii by 2 + 2 pso on Abd. IVsternum (versus 1 + 1), chaetae missing on Th. I sternum (versus present), fourchaetae on subcoxa 1 of leg I (versus two), and small axial chaeta a0 on Abd. V(versus much longer and sometimes asymmetrical). The most notable characters of T.hainanica sp. nov. are short anal spines and very long chaeta a0 on Abd. VI.

Thalassaphorura duplopunctata (Strenzke 1954)(Figures 5 and 6)

Material examined

Thirteen females and 13 males, Zhifu island, 37°36′N, 121°24′E, shingly beach (No.23–26, 28–34, 40–42, 45–47), Yantai City, 21 April 2011, leg. Y. Bu, C.W. Huang, M.B. Potapov and N.A. Kuznetsova; 2 males, Yangma island, 37°27′N, 121°36′E,shingly beach (No. 70), 22 April 2011, leg. Y. Bu, C.W. Huang, M.B. Potapov and


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Figure 5. Thalassaphorura duplopunctata (Strenzke 1954). (A) Postantennal organ; (B) organof Ant. III; (C) dorsal chaetotaxy of head and Th. I–II; (D) dorsal chaetotaxy of Th. III–Abd. VI (female); (E) dorsal chaetotaxy of Abd. III–VI (male). Scale bars: 100 µm (C–E),10 µm (A, B).

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N.A. Kuznetsova. 20 individuals (10 females and 10 males) are deposited in SIPPE, 2(1 female and 1 male) in MSPU, and 4 (2 females and 2 males) in NEIGAE.

We also studied the materials of populations of T. duplopunctata from severallocations in the northern European part of Russia (Murmansk coast and DolgyIsland) and Far East (coast near Magadan), all leg. Babenko.

Description based on Chinese specimens

Size 1300–1460 µm in females, 1100–1350 µm in males. Body subcylindrical, bodysides almost parallel.

Pseudocellar formula: 32/233/33343 dorsally, 11/000/01110 ventrally (Figures5C–E, 6D), subcoxa 1 of legs I–III with two, two and two pso respectively.

Figure 6. Thalassaphorura duplopunctata (Strenzke 1954). (A) Labial palp; (B) labrum; (C)antenna; (D) ventral side of Abd. II–VI; (E) tibiotarsus III. Scale bars: 100 µm (C, D,), 10 µm(A, B, E).


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Parapseudocelli absent. Pseudopore formula: 00/011/11110 dorsally, 00/111/000x00ventrally.

S-chaetae not distinguishable from ordinary chaetae. Tiny and blunt ms, presenton Th. II–III.

Head. Antennae slightly longer than head. Length ratio of Ant. I : II : III : IV asabout 1 : 2 : 2 : 2.5. Ant. IV with subapical organite with apex globular; basolateral ms atabout half length from base (Figure 6C). Ant. III sensory organ composed of fivepapillae, five guard chaetae, two small sensory rods and two smooth subequal clubs,and a lateral ms (Figure 5B). Ant. II with 13 chaetae. Ant. I with nine chaetae. Antennalbase with distinct granulation. PAO composed 18–22 simple vesicles (Figure 5A). Dorsalcephalic chaeta d0 present. 3 + 3 p-chaetae present between two inner posterior pso, p1anterior to others (Figure 5C). Mandible with strong molar plate and four apical teeth.Maxilla bearing three teeth and six lamellae.Maxillary outer lobe with a simple palp, onebasal chaeta and two sublobal hairs. Labral chaetae formula 4/142 (Figure 6B). Labiumwith six proximal, four basomedian (E, F, G, f) and six basolateral (a, b, c, d, e, e’)chaetae; labial type AC, papillae A–E respectively with 1, 4, 0, 3 and 2 guard chaetae(Figure 6A). Postlabial chaetae 4 + 4 along ventral groove.

Body chaetotaxy (Figures 5C–E, and 6D). Ordinary chaetae differentiated inmesochaetae and macrochaetae. Th. I tergum with 7–8 + 7–8 chaetae. Th. II–IIIterga with 4 + 4 chaetae and Abd. I–II terga with 3 + 3 chaetae respectively onboth side of axial line, without axial chaeta. Chaetae of Abd. III–V terga asymme-trical (more pronounced in males), Abd. VI tergum with one axial chaeta (m0)(Figure 5D, E). Th. I, II and III sterna with 1 + 1, 1 + 1, 1 + 1 chaetae respectively.

Appendages. Subcoxa 1 of legs I–III with 4, 4 and 4 chaetae, subcoxa 2 with 1, 4and 4 chaetae, respectively. Tibiotarsi of legs I, II and III with 18 (1, 8, 9) chaetaeeach. Unguis without teeth. Unguiculus 0.7 times as long as inner edge of unguis,with inner basal lamella (Figure 6E). Ventral tube with 1 + 1 anterior chaetae, 6–8 + 6–8 distal chaetae, 2 + 2 basal chaetae. Furca reduced to a field of finegranulation and with four small dental chaetae arranged in two rows below; onlyone manubrial row of chaetae present (Figure 6D).

Genital plate with 16–18 chaetae in females, 30–52 chaetae in males. Male organabsent. Anal valves with numerous acuminate chaetae; each lateral valve with a0 and2a1; upper valves with chaetae a0, 2b1, 2b2, c0, 2c1, 2c2. Anal spines set on distinctpapillae, 0.7 times as long as inner edge of hind unguis.

Variation

Two females from China were found with additional pso on the ventral side of Abd.IV (only on one half in one of the females).

Ecology

From the middle part of intertidal zone to the supralittoral part of shingly beaches.

Remarks

Thalassaphorura duplopunctata is distributed in the Arctic and boreal areas of theHolarctic. Its scarce records in Eastern Palaearctic and Nearctic are probably the

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result of insufficient knowledge of littoral Collembola of the northern Pacific com-pared with respective areas of the Atlantic, which have been studied in more detail(Figure 7). Considering Shandong Province to be the most southern record of thisprimarily northerly distributed species, we give its full description here.

Figure 7. Records of Thalassaphorura duplopunctata. Published data are used after Babenkoand Fjellberg (2006); Strenzke (1954); Fjellberg (2007); Fjellberg (1998), Pomorski andSkarżyński (2001), Babenko (2012). Numerous records of the species in Spitsbergen andsome neighboring areas were not used since they block others. The exact locations inGreenland and Northern Alaska were not specified (peculiarly marked on map).


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Thalassaphorura lifouensis (Thibaud and Weiner 1997)

Material examined

Fifteen females and 12 males, Zhujiajian island, 29°55′N, 122°25′E, sand beach (No.42, 44, 45, 47, 48), Zhoushan County, Ningbo City, Zhejiang Province, East China,13 April 2011, leg. Y.W. Huang and M.B. Potapov. 19 individuals (10 females and 9males) are deposited in SIPPE, 2 (1 female and 1 male) in MSPU, and 6 (4 femalesand 2 males) in NEIGAE.

Remarks

Thalassaphorura lifouensis was first described from beaches in New Caledonia(Thibaud and Weiner 1997). Our record considerably expands the distribution ofthe species.

Our littoral material fits the original description, except that a0 is absent on Abd.V tergum in our specimens.

Acknowledgements

The present study was supported by the National Natural Sciences Foundation of China(31301873) and NSFC-RFBR Cooperative Research Project (31111120077/11-04-91179-GFENa). We sincerely thank Y.X. Luan, Y. Bu, C.W. Huang (Shanghai) and N.A.Kuznetsova (Moscow) for their warm assistance during the collection. The work was alsosupported by the National Museum of Natural History (Paris). We also give our cordial thanksto Louis Deharveng and Anne Bedos (Paris) for providing favourable working conditions andBettine van Vuuren (South Africa) for linguistic corrections. We are much indebted to AnatolyBabenko (Moscow) for the loan of valuable material for T. duplopunctata.

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