ISSN 1226-9999 (print) ISSN 2287-7851 (online)

Korean J. Environ. Biol. 33(2) : 153~159 (2015) http://dx.doi.org/10.11626/KJEB.2015.33.2.153

Six Korean New Records of the Nais Species (Annelida, Clitellata, Naididae)

Jeounghee Lee1 and Jongwoo Jung1,2,*

1The Division of EcoCreative, Ewha Womans University, Seoul 120-750, Korea 2Department of Science Education, Ewha Womans University, Seoul 120-750, Korea

Abstract - The oligochaete worms in the genus Nais are common to freshwater habitats. These worms have a highly-developed prostomium and pigmented eye spots. All species have hair chaetae, bifid or single pointed needle chaetae on the dorsal side and ventral chaetae beginning in II with bifid crotchets. Most species of Nais genus live in areas where bottom is covered by sand, gravel or organic matter in aquatic plants. Currently, 26 species of Nais have been recorded worldwide. From the recent faunal studies, 3 species of Nais have been newly reported in Korea. Here, we newly report 6 species of Nais with diagnosis, illustrations and identification keys to Korean Nais species: N. behningi, N. pseudobtusa, N. simplex, N. bretscheri, N. stolci and N. elinguis.

Key words: Nais, Naididae, oligochaeta, Clitellata, Annelida, Korea

INTRODUCTION al. 2012). Most species of Nais have ventral bundles with bifid and sigmoid crotchets. Some species have giant chae­ Freshwater oligochaetes live in a broad range of aquatic tae in the ventral bundles of some segments. The dorsal environments worldwide and include about 1,100 species chaetae begin in segment VI and include long, thin hair of 13 families (Martin et al. 2008). The family Naididae chaetae, as well as short, bifid or single­ pointed needle chae- is a large group of freshwater oligochaete (Milbrink 1987; tae (Brinkhurst and Jamieson 1971). In this study, we newly Chapman 2001; Smutná et al. 2008). Of these the subfamily found 6 Nais species living in Korea. Naidinae appears in a wide range of habitats, ranging from rivers, pools, and estuaries (Timm and Martin 2015). These worms are generally smaller than other aquatic oligochaete MATERIALS AND METHODS families and they have a very soft body, pale body color and unique chaetae from other oligochaetes. Naidinae comprises We collected Nais specimens from fine sand and muddy 238 freshwater species (Martin et al. 2008) of which about sediment with high organic material at the waterside of 4 26 species belong to the genus Nais. Thirty-two species of locations in Korea (Jungrang-gu; Namyangju; Paju; Yang- Naididae have been reported from Korea with only 3 species yang) using a plankton hand net or hand shovel from April from the genus Nais: N. communis, N. variabilis, N. pardalis 2013 to September 2014. Samples have been brought to the (Jung 2011; Jung 2012; Park et al. 2013a, b; Lee and Jung laboratory while they were alive. Then, they were sorted 2014a, b). Key characteristics for identification of Nais spe- under the stereomicroscope (Motic, SMZ-168, Hong Kong). cies are the chaetae shape and number per bundle (Envall et For detailed observation, specimens were fixed in 5% form- aldehyde or 80% ethanol solution and mounted in Canada balsam according to the protocol described by Erséus in * ‌Corresponding author: Jongwoo Jung, Tel. 02-3277-2616,

Fax. 02-6937-0733, E-mail. [email protected] 1994. BX41 research microscope (Olympus, Tokyo, Japan)

ⓒ2015. Korean Society of Environmental Biology. 154 Jeounghee Lee and Jongwoo Jung attached with 650D digital camera (Canon, Tokyo, Japan) with sickle-shaped upper tooth; enormously as long as the was used for pictures. Measurements on pictures were per­ lower (Fig. 1A, B). Stomach beginning from VII. formed by using the image analyzing software, InnerView­ Remarks: N. behningi have a specific anterior ventral chae- TM-i series (Innerview Co. Ltd, Gyeonggi-do, Korea). tae resembles (or looks like) sickle-shaped not appeared from other species. Habitat: The sample was collected along the edges of stre­ RESULTS AND DISCUSSION am. Bottom of this site consists of sandy and gravel bottom with some water plants. Phylum Annelida Linnaeus, 1758 환형동물문 World distribution: Holarctic. Class Clitellata Linnaeus, 1740 환대강 Deposition: NIBR No. KOSPIV0000193710. Order Haplotaxida Grube, 1850 지렁이목 Identifiers: Jeounghee Lee, Jongwoo Jung. Family Naididae Ehrenberg, 1828 물지렁이과 Subfamily Naidinae Ehrenberg, 1828 물지렁이아과 2. Nais‌ pseudobtusa Piguet, 1906 머리털물지렁이 (신칭) Genus Nais Muller, 1773 물지렁이속 (Fig. 2A-D) Synonyms: Nais obtuse (Gervais) var. pseudobtusa Piguet. 1. Nais‌ behningi Michaelsen, 1923 큰낫물지렁이 (신칭) Piguet, 1906: 238. (Fig. 1A, B) Nais pseudobtusa Piguet. Piguet, 1909: 193. Synonyms: Nais behningi Michaelsen, 1923: 34. Material examined: Korea: 1, Geumchon-dong, Paju-si, Material examined: Korea: 1, Toegyewon-myeon, Nam­ Gyeonggi-do, 37˚45′59.37″N, 126˚46′27.01″E, 27 Aug yangju-si, Gyeonggi-do, 37˚38′33.01″N, 127˚9′1.65″E, 22 2013, collected by Lee JH. Sep 2013, collected by Lee JH. Diagnosis: Length 0.28 mm, width at V 0.03 mm, number Diagnosis: Length 0.18 mm, width at V 0.14 mm, number of segments 37. of segments 22. Eyes present. Dorsal bundles with 1~3 straight, long hairs Eyes present. Dorsal chaetae with hair and needle chaetae and long needle chaetae bearing distinct nodulus (Fig. 2A). 1~2 per bundle, needles thin and hair-like distally. Ventral Ventral chaetae by 2~5, upper tooth thinner than lower chaetae of II-V, 5~10 per bundle, with long, strong curved tooth and up to 1.5 times as long as lower (Fig. 2B, D); sli­

A B

Fig. 1. Nais behningi. A, Ventral chaetae bundle of XIX; B, Ventral chaetae of VI. Scale bars: A, B=3 μm. Six Korean New Records of the Nais Species 155

A B C D

Fig. 2. ‌Nais pseudobtusa. A, Needle chaetae of VII; B, ventral chaetae of IV; C, Ventral chaetae VI; D, Ventral chaetae of XIX. Scale bars: A-D=1 μm.

A B C

Fig. 3. Nais simplex. A, Needle chaetae X; B, Ventral chaetae VII; C, Ventral chaetae XXIII. Scale bars: A-C=3 μm. ghtly thicker from VI (Fig. 2C). gu, Seoul, 37˚34′52.87″N, 127˚4′41.74″E, 22 Sep 2013, col­ Remarks: N. pseudobtusa is hard to distinguish from Nais lected by Lee JH. simplex, N. barbata, N. alpine (Van Haaren T and J Soors, Diagnosis: Length 0.28 mm, and width at V 0.067 mm, num­ 2012). All worms have simple point needle tips. Dorsal ber of segments 29. needles in N. pseudobtusa are thinner, sharper tipped, and Dorsal hair chaetae and needles 1~2 per bundle, needles normally hair-like, as compared to other species. simple pointed (Fig. 3A). Ventral chaetae of II-V, 2~6 per Habitat: This species from the roots of waterweeds at the bundle, longer, straighter and thinner, with nodulus proximal edge of streams covered with sand or organic matter. and upper tooth nearly twice the length of the lower one (Fig. World distribution: Common, Asia, Africa, America, Eu- 3B, C). Dorsal vessel to the left of the middle line. Swims rope, Africa, Afghanistan. with spiral movements. Deposition: NIBR No. KOSPIV0000193709. Remarks: Nais simplex is very difficult to distinguish from Identifiers: Jeounghee Lee, Jongwoo Jung. N. pseudobtusa, N. barbata, N. alpina (Van Haaren and Soors 2012). N. simplex have round end tips, as compared 3. Nais‌ simplex Piguet, 1906 둥근털물지렁이 (신칭) with N. pseudobtusa. (Fig. 3A-C) Habitat: Bottom of collected site is sludge such as soft mud Synonyms: Nais variabilis var. simplex Piguet, 1906: 260. and organic matter. Nais simplex Piguet. Piguet, 1909: 202. World distribution: Europe, Asia, North America, South America. Material examined: Korea: 1, Myeonmok-dong, Jungrang- Deposition: NIBR No. KOSPIV0000206591. 156 Jeounghee Lee and Jongwoo Jung

Identifiers: Jeounghee Lee, Jongwoo Jung. Remarks: N. bretscheri has giant ventral chaetae from VII. Shape of upper teeth is very thick and straight, while lower 4. Nais‌ bretscheri Michaelsen, 1899 tooth is very short or reduced. This worm is often confused 큰손물지렁이 (신칭) (Fig. 4A-D) with N. pardalis which have giant chaetae from VI, whereas Synonyms: Nais bretscheri Michaelsen, 1899: 121. those in N. bretscheri start from VII. Habitat: This site is up the river which is clear, cool and Material examined: Korea: 1, Beopsuchi-ri, Hyeonbuk- shallow water. The streambed consists of various types of myeon, Yangyang-gun, Gangwon-do, 37˚53′57.89″N, 128˚ sand with some organic matter. 36′51.57″E, 9 Sep 2014, collected by Lee JH. World distribution: Cosmopolitan. Diagnosis: Length 0.14 mm, width at V 0.019 mm, number Deposition: NIBR No. KOSPIV0000216560. of segments 14. Identifiers: Jeounghee Lee, Jongwoo Jung. Eyes present. Dorsal chaetae and needles 1~2 per bun- dle; hair chaetae single, short, 1~2 needle, with quite long 5. Nais‌ stolci Hrabe, 1981 작은손물지렁이 (신칭) parallel teeth (Fig. 4A, D). Ventral chaetae of II-V, 4~6 per (Fig. 5A-C) bundle, thin and straight, with upper tooth about double the Synonyms: Nais stolci Hrabe, 1981: 33. length of lower; those of the following segments 1~6 per bundle (Fig. 4C). Giant chaetae beginning from VII, 2 per Material examined: Korea: 1, Beopsuchi-ri, Hyeonbuk- bundle, thick, straight, and very short (Fig. 4B). myeon, Yangyang-gun, Gangwon-do, 37˚53′57.89″N, 128˚

A B C D

Fig. 4. Nais bretscheri. A, Body form; B, Giant chaetae VII; C, Ventral chaeta; D, Dorsal chaetae. Scale bars: A=2 μm, B-D=5 μm.

A B C

Fig. 5. Nais stolci. A, Ventral chaetae III; B, Ventral chaetae VII, VIII; C, Dorsal needle III. Scale bars: A-C=10 μm. Six Korean New Records of the Nais Species 157

A B C D

Fig. 6. ‌Nais elinguis. A, Dorsal chaetae of VII; B, Dorsal chaetae of XI; C, Ventral bundles of III; D, ventral chaetae of VII. Scale bars: A-C=10 μm

36′51.57″E, 9 Sep 2014, collected by Lee JH. Material examined: Korea: 1, Toegyewon-myeon, Nam­ Diagnosis: Length 0.162 mm, width at V 0.043 mm, num- yangju-si, Gyeonggi-do, 37˚38′33.01″N, 127˚9′1.65″E, 22 ber of segments 24. Sep 2013, collected by Lee JH. In II-V ventral chaetae by 3~5 with upper tooth twice as Diagnosis: Length 0.10 mm, width at V 0.013 mm, number long. From VI on, 3~4 enlarged chaetae per bundle, upper of segments 12. tooth up to 4 times longer (Fig. 5A, B). Dorsal chaetae be- Dorsal chaetae 1~2 hairs and needles 1~3 per bundle, ginning in VI, including 1 hair, 1~2 needle with long par­ long parallel teeth (Fig. 6A, B). Ventral chaetae 2~5 per allel teeth (Fig. 5C). bundle, with upper tooth 1.5~2 longer and thinner than low­ Remarks: Specimens of posterior ventral chaetae shape er (Fig. 6C, D). Swims with lateral movements. looked similar to N. pardalis or N. bretsheri. They have gi- Remarks: Previous studies, this species is frequently found ant chaetae. N. bretsheri have giant chaetae from VII, while in brackish water, abundant in organically enriched sediment. N. pardalis and N. stolci beginning from VI. Hair chaetae But this specimen collected in relatively clean water with of N. stolci are longer than N. pardalis. So, these chaetae some organic sediment. shapes correspond with those of N. stolci. This is the first Habitat: The sample was collected along the edges of stre­ report on this species from Asia. am. Bottom of this site consists of sandy and gravel bottom Habitat: This site is up the river which is clear, cool and with some water plants. shallow water. The streambed consists of various types of World distribution: Cosmopolitan. sand with some organic matter. Deposition: NIBR No. KOSPIV0000216623. World distribution: Europe. Identifiers: Jeounghee Lee, Jongwoo Jung. Deposition: NIBR No. KOSPIV0000216600. Identifiers: Jeounghee Lee, Jongwoo Jung. 8. Nais communis Piguet, 1906 보통물지렁이 Synonyms: Nais communis Piguet, 1906: 247. 6. Nais pardalis Piguet, 1906 시골물지렁이 Nais communis Park et al., 2013a: 511. Synonyms: Nais pardalis Piguet, 1906: 253. Nais pardalis Park et al., 2013a: 511. 9. Nais variabilils Piguet, 1906 물지렁이 Synonyms: Nais variabilis Piguet, 1906: 253. 7. Nais‌ elinguis Müller, 1773 하천물지렁이 (신칭) Nais variabilis Jung, 2011: 408. (Fig. 6A-C) Synonyms: Nais elinguis Müller, 1773: 22. 158 Jeounghee Lee and Jongwoo Jung

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We would like to thank Christer Erséus (Gothenburg, imalium infusoriorum, helminthicorum et testaceorum, non

Sweden), and Patrick Martin (Brussel, Belgium) for their marinorum, succincta historia / auctore Othone Friderico kind information on the habitat conditions of specimens, Müller. et Lipsiae : apud Heineck et Faber. Six Korean New Records of the Nais Species 159

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