Anim. Syst. Evol. Divers. Vol. 34, No. 1: 3-9, January 2018 https://doi.org/10.5635/ASED.2018.34.1.041

Review article New Records of the Genus (Collembola: ) from Korea

Hakseo Kim, Kyung-Hwa Park*

Department of Biology Education, Institute of Science Education and Institute of Fusion Science, Chonbuk National University, Jeonju 54896, Korea

ABSTRACT

Two species of the genus Isotomurus Börner are newly recorded in Korea; I. bimus Christiansen and Bellinger, and I. plumosus Bagnall. These species are collected from salt marshes near West Sea of Korea. The Korean materials of I. bimus agreed well with the original description by Christiansen and Bellinger from North America, in its peculiar body pattern, with two long ciliated setae on tibiotarsus of hind leg, multisetaceous lateral flap of ventral tube and the presence of a mucronal lateral seta. Isotomurus plumosus is also easily identified from other Isotomurus species by the peculiar colour pattern, and the presence of long maxillary lamella 1 and a mucronal seta. Keywords: Isotomurus bimus, Isotomurus plumosus, , hygrophilous, salt marsh,

INTORODUCTION marshes near West Sea.

The collembola are uaually associated with soil and leaf litter, but they are often found in special habitats such as MATERIALS AND METHODS caves, ant or termite nests, and marine and fresh water litto- ral zones (Lee and Park, 1986; Greenslade, 1991; Kim and Our study is based on the samples collected during the ex- Lee, 2000; Park and Lee, 2000). pedition to various types of littoral regions in South Korea. Most Isotomurus Börner, 1903 species are hygrophilous Specimens were collected live by aspiration, and sometimes and aquatic species. They are usually found in different by pitfall trap. For microscopic study of entire individuals, kinds of damp sites and bank (Potapow, 2001). The genus specimens were preserved in 95% ethanol were cleared in Isotomurus Börner, 1903 may be easily recognized by (1) Marc André I fluid (Massoud, 1967), then mounted in Hoy- 8+8 ommatidia, (2) tibiotarsus without clavate tenent hair, er’s medium to prepare permanent slides. Slides were dried (3) the position of three macrochaetae on each side of ab- and hardened in a 60°C oven for 2-4 days. Specimens were dominal segment IV arranged in a triangular, and (4) abdom- examined with bright-field, differential interference-contrast inal tergites II-IV with trichobothria (except in Isotomurus (Nikon Eclipse 80i; Nikon, Tokyo, Japan), or phase-contrast antennalis Bagnall, 1940 and I. chaos Potapow & Babenko, microscopes (Nikon Eclipse 80i). Some specimens were 2011) (see Potapow, 2001; Fjellberg, 2007; Potapow and observed with a scanning electron microscope (SEM). For Babenko, 2011). Isotomurus are reported more than 50 spe- SEM observation, the specimens were chemically fixed in cies from all over the world, of which four species are known order to preserve as close as possible to native state. After from Korea (Shon, 1963; Yosii and Lee, 1963; Kim and Lee, they were fixed in 2.5% glutaraldehyde and 2% formalde- 2000): I. balteatus (Reuter, 1876), I. mankyungensis Kim hyde in phosphate buffered saline (PBS) for 2 h, post-fixing & Lee, 2000, I. palustris (Müller, 1776), and I. palustroides in 2% osmium tetroxide in PBS for 30 min (modified Kar- Folsom, 1937. novsky’s fixative). Then, they change to were dehydrated up In the present study, two species in the genus Isotomurus to 100% ethyl alcohol. It was dried in a desicator for 24 h, are newly recorded in Korea, which were collected in salt and then covered osmium. Observation was done with field

This is an Open Access article distributed under the terms of the Creative *To whom correspondence should be addressed Commons Attribution Non-Commercial License (http://creativecommons.org/ Tel: 82-63-270-2783, Fax: 82-63-270-2781 licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, E-mail: [email protected] and reproduction in any medium, provided the original work is properly cited. eISSN 2234-8190 Copyright The Korean Society of Systematic Zoology Hakseo Kim, Kyung-Hwa Park emission scanning electron microscope SUPRA 40VP in- long as, or slightly shorter than the diameter of ommatidium. stalled in the Center for University-Wide Research Facilities Labral setae 4/5,5,4; apical edge of labrum with 4 sharp (CURF) at Chonbuk National University, Jeonju, Korea. folds, anterior edge is uniformly ciliated (Fig. 1C). Maxilla Materials are deposited in the National Institute of Bio- with 3-toothed capitulum and 6 short lamellae. Maxillary logical Resources, Incheon, Republic of Korea (NIBR) and outer lobe with bifurcate and 4 sublobal setae (Fig. 1E). La- the Insect Collection of the Biology Education Department, bium with group of 7 proximal and 5-6 basomedial setae,

Chonbuk National University, Jeonju, Korea (CBNU). and guards; guard e7 present (Fig. 1D). Morphological abbreviations used in this paper are as Claws as common for the genus, with a pair of lateral follows: Abd I-VI, abdominal segments I-VI; Ant I-IV, seta (Fig. 2C, D). Unguis with 2 lateral and 1 outer teeth, antennal segments I-IV; PAO, postantennal organ; Th I-III, but without inner tooth. Unguiculus pointed, with lamella thoracic segments I-III. rounded basally and without inner tooth. Tibiotarsi of mid- and hind legs with 2 long ciliated setae respectively. Tenent hairs pointed, shorter than outer edge of unguis (Fig. 2D). SYSTEMATIC ACCOUNTS Ventral tube with 5+5 laterodistal setae, 20+20 anterial setae, more than 30 posterior setae. Retinaculum quadriden- Class Collembola Lubbock, 1870 tate with 10 setae. Order Börner, 1913 Furcula long and tapering. Ratio of manubrium to dens Superfamily Isotomoidea Szeptycki, 1979 as related as about 1 : 1.8-2.0. Marginal thickening simple, Family Isotomidea Schäffer, 1896 with 1+1 internal spine. Dens intensely hirsute ventrally. Subfamily Isotomidea Schäffer, 1896 Dorsal pilose field on dens reaching approximately middle Genus Isotomurus Börner, 1903 part. Mucro quadridentate (Fig. 2E), with a lateral seta (Fig. 2F); large basal tooth with lamella. 1*Isotomurus bimus Christiansen & Bellinger, 1980 Body with dense cover of setae, with trichobothria on (Figs. 1, 2) Abd. II-IV and macrochaetae on Abd. IV-VI; abdominal Isotomurus bimus Christiansen & Bellinger, 1980: 679-689, macrochaetae long, densely ciliated. fig. 541. Distribution. North America (USA), Korea (new record). Remarks. The present materials agree well with the original Type locality. North America (Northwestern University description by Christiansen and Bellinger (1980) from North greenhouse). America, in its peculiar body pattern, with two long ciliated Material examined. 3 males and 1 female on slide, Korea, setae on tibiotarsus of hind leg, and multisetaceous lateral Jeollabuk-do: Buan-gun, Haseo-myeon, Jangsin-ri, 126°36ʹ flap of ventral tube as well as presence of a mucronal lateral 35ʺN, 35°44ʹ03ʺE, collected from debris on reedy salt marsh, seta. This species is also similar to I. punciferus Yosii, 1963 20 Aug 2014, Leg. Park KH, Kim HS, Lee I. in body pattern, however, different from the members of I. Description. Body length up to 1.6-1.8 mm. Body shape as punciferus by absence or presence of inner tooth on unguic- common for the genus. Abd. V and Abd. VI separated (Fig. ulus (presence in original description) and by relative size of 1A). PAO (longer in original description). Background color yellowish white. Head with front trans- verse band connection eye-spots and median patch in a 2*Isotomurus plumosus Bagnall, 1940 (Figs. 3, 4) posterior position. Body with distinct narrow longitudinal Isotomurus plumosus Bagnall, 1940: 101. middorsal dark line on Th. II-Abd. III, all segments with Isotomurus plumosus: Fjellberg, 2007: 97, fig. 59I, 60D, transverse bands. Abd. II-Abd. IV with 3+3, 3+3, 1+1 60K. small black spots marking the base of trichobothrium. Antenna : head=1.8-1.9 : 1; Ant. I with a group of 5-6 Type locality. Gr. Britain (Hysker Island, Northumberland short ventroapical sensilla; Ant. II and Ant. IV with several and Cheshire). curved sensilla; sense organ of Ant. III normal (Fig. 1B), Material examined. 2 males on slide, Korea: Jeollabuk-do: with short blunt, and short and long pointed sensilla; subapi- Buan-gun, Haseo-myeon, Baekryeon-ri, Weolpo, 126°35ʹ cal pin-seta of Ant. IV present. 40ʺN, 35°43ʹ09ʺE, collected from moss growing on rock in Eyes 8+8 ommatidia on each, equal in shape (Fig. 2A); salt marsh, 1 Oct 2014, Park KH, Kim HS, Lee I. leg. pigment present. Postantennal organ elliptical (Fig. 2B), as Description. Body length up to 2.0-2.5 mm. Ground color

Korean name: 1*점박이늪마디톡토기, 2*털보늪마디톡토기

4 Anim. Syst. Evol. Divers. 34(1), 3-9 New Records of Isotomurus from Korea

A B

C

D E

Fig. 1. Isotomurus bimus Christiansen & Bellinger. A, Body shape; B, Sense organ of Ant. III; C, Labrum; D, Labial palp; E, Maxil- lary outer lobe. Scale bars: B, E=2 μm, C=10 μm, D=3 μm. yellowish with sharp broad mid-dorsal band and lateral with a group of 4 short ventroapical sensilla. Ant. III organ patches from Th. II to Abd. VI. Head with anterior transver- normal, with short and long sensilla (Fig. 3C). sal band and posterior spot (Fig. 3A). Eyes 8+8 ommatidia on each, equal in shape (Fig. 3B); Antennae 1.7 times longer than head length. Antennal pigment present. Postantennal organ elliptical, slightly lon- segments I-IV ratio as 1.0 : 1.8 : 1.9-2.0 : 2.1-2.4. Ant. I ger than the diameter of ommatidium.

Anim. Syst. Evol. Divers. 34(1), 3-9 5 Hakseo Kim, Kyung-Hwa Park

A B

C D

E F

Fig. 2. Isotomurus bimus Christiansen & Bellinger. A, Eyes; B, Postantennal organ; C, Claw; D, Distal part of Leg. III; E, Mucro (latral); F, Mucro (dorsal). Scale bars: A, C=10 μm, B, E, F=2 μm, D=20 μm.

Labral setae 4/5,5,4; apical edge of labrum with 4 sharp papillae and 16 guards. Labium with group of 9 proximal folds, anterior edge is uniformly ciliated (Fig. 3D). Maxilla and 7 basomedial setae (Fig. 3E). with 3-toothed capitulum and 6 short lamellae, lamella 1 Claw shape as common for the genus with a pair of lateral much longer than capitulum. Maxillary outer lobe with seta (Fig. 4A). Unguis without inner tooth, but with 2 lateral bifurcate and 4 sublobal setae. Labial palp with all apical and 1 outer teeth. Unguiculus pointed with lamella round-

6 Anim. Syst. Evol. Divers. 34(1), 3-9 New Records of Isotomurus from Korea

A B

C

D E

Fig. 3. Isotomurus plumosus Bagnall. A, Body shape; B, Eyes; C, Sense organ of Ant. III; D, Labrum; E, Labial palp. Scale bars: B-D=10 μm, E=3 μm. ed basally and without inner tooth (Fig. 4A). Tenent hairs Furcula long and tapering. Ratio of manubrium to dens pointed, longer than outer edge of unguis. as related as about 1 : 2.0-2.1. Manubrium and dens with Ventral tube with 6-9 laterodistal setae, 12-14 anterial numerous setae on all side. Manubium with sharp ventroap- setae, 20 or more posterior setae (Fig. 4B). Retinaculum ical teeth (Fig. 4D). Dens narrow and crenulated (Fig. 4E), quadridentate with 12 setae (Fig. 4C). dorsal pilose field on dens extends more than halfway (ap-

Anim. Syst. Evol. Divers. 34(1), 3-9 7 Hakseo Kim, Kyung-Hwa Park

A B

C D

E F

Fig. 4. Isotomurus plumosus Bagnall. A, Claw; B, Ventral tube (lateral part); C, Retinaculum; D, Manubium; E, Dens; F, Mucro. Scale bars: A, C=10 μm, B, E=20 μm, D, F=2 μm. proximately to 3/4 from base). Mucro quadridentate, with a ated. lateral seta and lamella on large basal tooth (Fig. 4F). Distribution. Palaearctic (Korea: new record). Body with dense cover of setae, with trichobothria on Abd. Remarks. This species is easily distinguished by peculiar II-IV and macrochaetae on Abd. IV-VI; abdominal macro- color pattern with the sharp broad mid-dorsal band, the chaetae long, densely ciliated. Short setae on abdomen cili- presence of several setae on laterodistal part of the ventral

8 Anim. Syst. Evol. Divers. 34(1), 3-9 New Records of Isotomurus from Korea tube, and the presence of long maxillary lamella 1 and a lat- Lee BH, Park KH, 1986. Three new species of Onychiuridae eral seta on mucro. (Collembola) from a Korean cave. Korean Journal of Sys- tematic Zoology, 2:11-20. Massoud Z, 1967. Monographie des Neanuridae, Collemboles ACKNOWLEDGMENTS Poduromorphes à pièces buccales modifiées. In: Biologie de l’Amérique Australe, III (Eds., Delamare Deboutteville C, Rapoport EH). CNRS, Paris, pp. 7-399. This work was supported by a grant from the National Müller OF, 1776. Zoologiae Danicae prodromus. Typiis Hallag- Institute of Biological Resources (NIBR), funded by the eriis, Hafniae, pp. 183-184. Ministry of Environment (MOE) of the Republic of Korea Park KH, Lee BH, 2000. Six Collembolan species (Insecta) (NIBR201301203; NIBR201501203). new to Korea, including two species from ant nests. Korean Journal of Systematic Zoology, 16:227-237. Potapow M, 2001. Isotomidae. In: Synopses on Palaearctic REFERENCES Collembola. Vol. III (Ed., Dunger W). Staatliches Museum Für Natuekunde Görlitz, p. 323.

Bagnall RS, 1940. Notes on British Collembola. VII. Entomol- Potapow M, Babenko AB, 2011. A new spiecies of Isotomurus ogists Monthly Magazine, 76:97-102. (Collembola: Isotomidea) without trichobothria. Russian Christiansen KA, Bellinger PF, 1980. The Collembola of North Entomological Journal, 20:113-117. America. North of the Rio Grande. Part 2. Families Ony- Reuter OM, 1876. Catalogus praecursorius Poduridarum Fen- chiuridae and Isotomidae. Grinnell College, Grinnell, IW, niae. Meddelanden of Societas Pro Fauna et Flora Fennica, pp. 387-784. 1:78-86. Fjellberg A, 2007. The Collembola of Fennoscandia and Den- Shon YT, 1963. Collembola from Korea. Treatises of the Seong­ mark. Part. II. Entomobryomorpha and Symphypleona In: gyungwan University, 8:312-322. Fauna Entomologica Scadinavica. Vol. 42. Brill, Leiden, Yosii R, 1963. On some Collembola of Hindukush, with notes pp. 1-264. on BOURLET and its allies. Result of the Kyoto Folsom JW, 1937. Nearctic Collembola or , of the University Scientific Expedition to the Karakoram and family Isotomidae. Smithsonian Institution the United Hindukush, 1955, Vol. IV, Insect Fauna of Afghanistan States National Museum Bulletin, 168:1-144. and Hindukush, Art. I. Kyoto University, Committee of the Greenslade PJ, 1991. Collembola (springtails). In: The insects Kyoto University Scientific Expedition to the Karakoram of Australia: a textbook for students and research workers and Hindukush, Kyoto, pp. 3-42. (Ed., Commonwealth Scientific and Industrial Research Yosii R, Lee CE, 1963. On some Collembola of Korea, with Organization). Vol. 1. Melbourne University Press, Carlton, notes on the genus Ptenothrix. Contributions from the Bio- pp. 252-263. logical Laboratory, Kyoto University, 15:1-37. Kim JT, Lee BH, 2000. Systematic study on aquatic Collembola (Insecta) from Mankyung River System of Korea. Korean Received September 29, 2017 Journal of Entomology, 30:179-185. Accepted January 4, 2018

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