Aquacult.Sci. 65(4)，409−415（2017）

Age and growth of the torrent in the Kawahara River of the Chikugo River system, Kyushu Island, Japan

1,＊ 2 2 2 Naohiko TAKESHITA , Kazuhiro SAKATA , Takuya KONDOU , Shingo NAGATA , 3 4 Akira ARAKI and Kazuo HOSHINO

Abstract: Ageand growth of thetorrentcatfish Liobagrus reinii from theKawahara Riverin the Chikugo River system, Kyushu Island, Japan were studied by examination of the vertebral centrum. A total of 289 specimens were caught between April and December 2000. Marginal increments of the vertebral centrum formed annual rings in June, and the spawning period took place from May to July (mainly in June). Sexual size dimorphism was not recognized, the growth of this fish is

expressed by the von Bertalanffy equation as Lt = 127.4[1-exp{-0.434(t+0.537)}] for both sexes,

where Lt is standard length in mm and t is age in years. This equation indicated that this catfish reached mean standard lengths of 62.0, 85.0 and 100.0 mm at 1 to 3 years old, respectively.

Key words: Age, Growth, Liobagrus reinii, Torrent catfish, Chikugo River system

Eight species of freshwater Siluriformes fish (Katano et al. 2006) and eggs and development (4 of thegenus Tachysurus,3ofSilurus and 1 of of larvae and juveniles (Nakatani et al. 2009) Liobagrus) inhabit theJapaneseArchipelago have been reported. However, little is known (Hosoya 2013). Thetorrentcatfish, Liobagrus about theageand growth of this catfish. reinii Hilgendorf, 1878 (Fig. 1), is an endemic Therefore, the purpose of this paper is to clarify species in Japan, and distributed in the rivers of theageand growth of L. reinii using specimens Kyushu, Shikoku and Honshu Islands with the collected in the Kawahara River of the Chikugo northern limit of Miyagi and Akita Prefectures River system, for the future conservation of this (Nakamura 1963; Miyadi et al. 1976; Hoshino et fish. al. 1996; Hosoya 2013). This species has been designated as a “vulnerable species” by the Ministry of theEnvironment(Ministry of the Environment 2015). Whereas, there are some reports where this catfish is caught for human consumption in mountain regions (Miyadi et al. 1976; Miyazaki and Kakuma 2001). Therearesomestudieson theecologyof Fig. 1. Liobagrus reinii (ca. 105 mm SL) in the L. reinii, reproductive ecology (Watanabe Kawahara River. 1994b), summer daytime habitat and population density (Katano et al. 2005), stomach contents

Received 10 July 2017; Accepted 16 October 2017. 1 Graduate School of Fisheries Science, National Fisheries University, Shimonoseki, Yamaguchi 759-6595, Japan. 2 West Japan Engineering Consultants, Co., Ltd., 1-1-1 Watanabe-dori, Fukuoka 810-0004, Japan. 3 Department of Applied Aquabiology, National Fisheries University, Shimonoseki, Yamaguchi 759-6595, Japan. 4 Oita MarinePalaceAquarium UMITAMAGO, Takasaki-yama-shita-kaigan, Oita 870 -0802, Japan. ＊Corresponding author: Tel, (+81)83-277-3943; E-mail, [email protected] (N. Takeshita). 410 N. Takeshita, K. Sakata, T. Kondou, S. Nagata, A. Araki and K. Hohino

0.01 g. The first four vertebrae of L. reinii are Materials and Methods fused and form the Weberian apparatus. In this study the sixth vertebrae were used for age Fieldwork was conducted each month from determination and growth analysis. These April to December 2000, in a 100 m stretch, vertebrae were soaked in 2% potassium hydrox- varying 7-16 m wide, of the Kawahara River (33° idesolution, followedby staining with a dash of 07’14”N, 130°57’59”E) a tributary of theChikugo alizarin red S, for 2 hours. After the staining, River system, Oita Prefecture, Kyushu Island, vertebrae were soaked again, they were further Japan (Fig. 2). Thestreamtypein thestudy area soaked in 2% potassium hydroxidesolution for 2 is classified as Aa, according to Kani’s classifica- days in orderto makethemuscletissue tion (Kani 1944). The riverbed consisted of transparent. Then the remaining muscle tissue boulders and cobbles in riffles and cobbles and was removed from the vertebrae using a fine gravel in pools. The catfish were captured by brush. The vertebrae were cut into 2 parts along hand net using a mask and snorkel by 5 persons the central longitudinal line. The focus, verte- during ca. 2 hours. Water temperature ranged bral centrum radii and ring radii on the right from 7.3 °C in winter (December) to 21.0°C in posterior part of the vertebrae (Fig. 3) were summer (July). photographed under a binocular microscope A total of 289 specimens were caught and (SMZ-1500, Nikon), and measured with image preserved in 10% buffered formalin, the speci- analysis software(Mac SCOPE, Mitani). mens were measured to the nearest 0.1 mm in Of the 205 vertebrae examined from speci- standard length (SL) and weighed to the nearest mens over 45mm SL, all of the vertebrae were readable. Sections of the vertebral centrum showed clear bands alternating with opaque narrow bands (Fig. 3). In the present study, the ring marks were defined as the outer bounda- ries of the clear bands. Marginal growth of the vertebral centrum was examined using a marginal growth index (MGI) to estimatetheperiodof ring formation, in the 205 specimens, which had 1-3 ring marks. The marginal growth index was calculated as:

MGI = 100 (R-rn)/(rn-rn-1)

Where R is centrum radius in mm, rn is the n-th

Fig. 3. Ring marks on the vertebral centrum of maleof Liobagrus reinii (106.8 mm SL) caught in theKawahara Riverin April 2000. F, focus; R, Fig. 2. Location of thestudy areain theKawahara Riverof centrum radius; r1 -r2, ring radii 1-2. Scalebar the Chikugo River system. indicates 0.5 mm. Ageand growth of Liobagrus reinii 411 ring radius (most outer ring mark) in mm. July in the 2 ring group. In subsequent months, Gonads were weighed to the nearest 1 mg. the values increased. Also, new ring marks were The gonadosomatic index (GSI) used to deter- formed at 0% (n = 13) in April, 26.7% (n = 15) in minethemonth of spawning, was calculatedas: May, 90.3% (n = 31) in Juneand 100 % (n = 32) GSI = 100 (GW/BW) in July. These results indicate that ring marks Where GW is gonad weight (g) and BW is body on the vertebral centrums were formed once a weight (g). year in June. The ring marks can therefore be To get a reliable growth curve, accurate ages regarded as annual rings. were assigned to each individual following the non-linear least-squares method, and birth Spawning period month was defined as June as this corresponded Relationships between SL and GSI of males with the peak of GSI of females. The von and females of L. reinii caught from April to July Bertalanffy growth formula was fitted to the areshown in Fig. 5. GSI over80 mm SL for relationship between SL and age using the non- males and those over 72 mm SL for females had linear least-squares method (KaleidaGraph high values. Monthly changes in the mean GSI v4.5.0, Synergy Software, USA) and defined by of 61 males and 96 females, sizes larger than 80 thefollowing equation: mm SL for males and 72 mm SL for females,

Lt = L∞[1-exp{-K(t+t0)}] sampled from April to December 2000, are

Where Lt is SL at age t and L∞, K,t0 arethe shown in Fig. 6. No clear tends were observes in asymptotic length, growth coefficient and hypo- the monthly changes in GSI for males. Whereas, thetical age at SL = 0, respectively. higher values of the GSI for females were

Results

Period of Ring Formation Monthly changes in the mean values of MGI in the1 ring group and 2 ring group areshown in Fig. 4. Low values of MGI appeared from Juneto July in the1 ring group, and from May to

Fig. 4. Monthly changes in marginal growth index (MGI) of vertebral centrum of Liobagrus reinii caught in the Kawahara River, from April to December 2000 ( ○ ,1 Fig. 5. Relationships between standard length and gonad ring group; ● , 2 ring group). Vertical lines indicate somatic index (GSI) of Liobagrus reinii caught in the standard deviations. Kawahara River from April to July 2000. 412 N. Takeshita, K. Sakata, T. Kondou, S. Nagata, A. Araki and K. Hohino

Fig. 6. Monthly changes in gonad somatic index (GSI) of Liobagrus reinii caught in theKawahara Riverfrom April to December 2000 ( ○ , male; ● , female). Vertical lines indicate standard deviations. observed from May to July with the maximum value in June. These results indicate that the spawning period for L. reinii in theKawahara River took place from May to July (mainly June), and shown close agreement with the period of ring formation.

Occurrence of yearlings and body size of males and females Monthly changes in SL frequency distribution of L. reinii caught from April to December are shown in Fig. 7. Thecatfish 45.1-107.8 mm SL were caught from April to July. Small sized fish (18.7-43.0 mm SL) were found in August. They could be estimated to be yearlings, because no annual ring marks were observed on the vertebral centrums of the specimens between 45-55 mm SL (n = 22) caught from September to December. The sizes of gonads for these Fig. 7. Monthly changes in standard length frequency specimens were very small, sex could not be distribution of Liobagrus reinii caught in theKawahara River from April to December 2000. determined under a binocular microscope. For 1-year-old class catfish captured from April to July, mean SL and standard deviation of P > 0.05; 2-year-old, P > 0.05). Maximum sizeof males were 57.2 ± 4.6 mm (n = 8), and females males was 106. 8 mm SL at age 2+ caught in were 54.9 ± 5.5 mm (n = 14), and for 2-year-old April, and that of females was 107.8 mm SL at class catfish, males were 85.1 ± 2.4 mm SL (n = age3 caught in June. 21), and females were 83.3 ± 4.6mm SL (n = 50). The sizes of both genders for the 1-year-old Growth equation class and 2-year-old class L. reinii were similar, Sexual size dimorphism was not recognized in respectively (Mann-Whitney U-test; 1-year-old, L. reinii, all specimens (n = 289) were used for Ageand growth of Liobagrus reinii 413

maximum sizes of T. nudiceps in theKoya River recorded were 295 mm SL for males and 173 mm SL for females (Takeshita et al. 2012). T. tokiensis in a test pond maintained by groundwater from the Sagami River exhibited marked sexual dimorphism, with males being larger than females (Suguro et al. 2011). Female T. tokiensis generally grow up to a maximum of approximately 150 mm SL, although individuals larger than 120 mm were rare, while males exceeding 200 mm were often observed during the study period (Suguro et al. 2011). It seems that T. ichikawai, T. aurantiacus and T. nudiceps Fig. 8. Standard length-at-age and the von Bertalanffy which spawn in nests (Watanabe 1994c; Mizoiri growth curveof Liobagrus reinii caught in theKawahara 1997; Yamaneetal. 2004; Matsuo and Takahama River from April to December 2000. 2004) have characteristics of sexual size dimor- phism of which males are larger than females calculation of thegrowth equation.Thegrowth (Watanabe 1994b; Takeshita et al. 1998; 2012). of this catfish was expressed by the von Whereas, for Silurus asotus paired females Bertalanffy equation for both genders as follows: were significantly larger than paired males in 2 Lt=127.4[1-exp{-0.434(t+0.537)}] (r = 0.937, the temporary waters around paddy field in t ≦ 3) Kyoto Prefecture (Katano et al. 1988), and Lake This equation indicates that L. reinii reaches Biwa, (Maehata 2002b; 2007). Also, paired mean SLs of 62.0, 85.0 and 100.0 mm at 1 to 3 females were significantly larger than paired years old, respectively (Fig. 8). males for S. lithophilus in LakeBiwa (Maehata 2001b). For S. biwaensis males of 40-80 cm in Discussion total length (TL) and females of 50-100 cm TL occurred in the spawning ground in Lake Biwa Growth and body size of males and females (Maehata et al. 1990). It seems that females are In our study, sexual size dimorphism was not larger than males, for the scatter-spawning recognized for L. reinii. Thegrowth of this catfish of S. asotus, S. lithophilus and catfish was expressed by the von Bertalanffy S. biwaensis (Katano et al. 1988; Maehata 2001a; equation, this equation indicates that this catfish 2001b; 2002a; 2002b; 2007; Maehata et al. 1990). grows to mean SLs of 62.0, 85.0 and 100.0 mm at Males of L. reinii are observed to guard eggs 1 to 3 years old. found under the boulders (Watanabe 1994b; Body sizes of males and females in the other Nakatani et al. 2009). Also, Watanabe (1994b) seven species of freshwater Siluriformes fish (4 reported that one male of this catfish guarded Tachysurus, and 3 Silurus) in Japan arealready 182 eggs and these eggs might have been reported. The maximum sizes of Tachysurus deposited by 2 or 3 females based on the ichikawai in the Tagiri River recorded were estimation from the fecundity of other river 108.0 mm SL for males and 93. 5 mm SL for females. However although this observation females (Watanabe 1994a). Sexual size dimor- suggests that the mating system in L. reinii is phism was apparent in immature, 1-year-old, and polygamous, sexual size dimorphism in this becoming more pronounced in older fish catfish was not recognized. It seemed that the (Watanabe1994a). Themaximum sizesof characteristic of similar body sizes in both sexes T. aurantiacus in the Chikugo River recorded was different from that shown in Tachysurus,of were 230.1 mm SL for males and 182.5 mm SL which males are larger than females. for females (Takeshita et al. 1998). Also, the 414 N. Takeshita, K. Sakata, T. Kondou, S. Nagata, A. Araki and K. Hohino

(Siluriformes: ) in an aquarium. Japan. J. Acknowledgments Ichthyol., 51, 169-174 (in Japanese with English abstract). Ministry of the Environment (2015) Red lists of brackish We extend our particular appreciation to the and freshwater fishes in Ministry of the Environment members of Tsue fisheries cooperative associa- 2015, in http://www.env.go.jp/press/files/jp/28060. tion for their variable information. pdf, accessed 21 April 2017 (in Japanese). Miyadi, D., H. Kawanabeand N. Mizuno (1976) Liobagrus reini.In“Colored illustrations of the freshwater fishes of References Japan ”, Hoikusha, Osaka, pp. 262-263 (in Japanese). Miyazaki, Y. and T. Kakuma (2001) Liobagrus reinii Hoshino, K., T. Matsuo and K. Hosoya (1996) Distribution fishing. In “The secrets of a fisherman in the Niyodo of Liobagrus reini (Siluriformes: ) in River”, Shogakkan, Tokyo, pp. 223-233. (in Japanese). Kyushu, Japan. Japan. J. Ichthyol., 43, 105-108 (in Mizoiri S. (1997) Geographical distribution and life history Japanese with English abstract). of theJapanesebagrid, Pseudobagrus aurantiacus Hosoya, K. (2013) Siluriformes, In “Fishes of Japan with (Temminck and Schlegel). A doctoral thesis, Nagasaki pictorial keys to the species 3rd edition” (ed. By T. University, pp. 1-111. Nakabo), Tokai University Press, Hatano, pp. 335-342 Nakamura, M. (1963) Liobagrus reini.In“Key to the (in Japanese). freshwater fishes of Japan fully illustrated in color”, Kani, T. (1944) Ecology of torrent-inhabiting insects. In Hokuryukan, Tokyo, p. 169 (in Japanese). “Insects I” (ed. By H. Furukawa), Kenkyusha, Tokyo, Nakatani, M., R. Inui, M. Kawagishi, J. Nakajima and N. pp. 171-317. Onikura (2009) Eggs and the development of larvae Katano, O., K. Saitoh and A. Koizumi (1988) Scatter- and juveniles of the torrent catfish, Liobagrus reini, spawning of thecatfish, Silurus asotus. Japan. J. from theKoishiwara River,a branch of theChikugo Ichthyol., 35, 203-211 (in Japanese with English River. Aquacult. Sci., 57, 315-320 (in Japanese with abstract). English abstract). Katano, O, T. Nakamura, S. Yamamoto and S. Abe(2005) Suguro, N., Y. Aizawa and K. Hosoya (2011) Natural Summer daytime habitat and population density of the propagation and growth of the endangered Japanese torrent catfish, Liobagrus reini, in theUrano River. bagrid catfish Pseudobagrus tokiensis in an ecological Ichthyol. Res., 52,50-56. test pond. Aquacult. Sci., 59, 265-273. Katano, O., T. Nakamura and S. Abe(2006) Stomach Takeshita, N., A. Araki, S. Mizoiri, O. Tabeta and S. Kimura contents of the torrent catfish Liobagrus reini in the (1998) Age, growth and maturity of the bagrid fish Urano River, Nagano Prefecture. Aquacult. Sci., 54, Pseudobagrus aurantiacus in theChikugo River, 225-226 (in Japanese with English abstract). Kyushu Island, Japan. Fish. Sci., 64,21-26. Maehata M. (2001a) The physical factor inducing spawn- Takeshita, N., K. Aoki, K. Yamabayashi and A. Araki (2012) ing of theBiwa catfish, Silurus biwaensis. Ichthyol. Res., Ageand growth of thebagrid catfish Pseudobagrus 48, 137-141. nudiceps in the Koya River, western Honshu Island, Maehata M. (2001b) Mating behavior of the rock catfish, Japan. Aquacult. Sci., 60, 371-376 (in Japanese with Silurus lithophilus. Ichthyol. Res., 48, 283-287. English abstract). Maehata, M. (2002a) Features of the reproductive ecology Watanabe, K. (1994a) Growth, maturity and population of therock catfish Silurus lithophilus. Ichthyol. Res., structureof thebagrid catfish, Pseudobagrus ichika- 49, 109-113. wai, in the Tagiri River, Mie Prefecture, Japan. Japan. Maehata, M. (2002b) Stereotyped sequence of mating J. Ichthyol., 41,15-22. behavior in the far eastern catfish, Silurus asotus, from Watanabe, K. (1994b) A notes on the reproductive ecology LakeBiwa. Ichthyol. Res., 49, 202-205. of thetorrentcatfish, Liobagrus reini (Siluriformes: Maehata, M. (2007) Reproductive ecology of the far Amblycipitidae). Japan. J. Ichthyol., 41, 219-221. eastern catfish, Silurus asotus (Siluridae), with a Watanabe, K. (1994c) Mating behavior and larval develop- comparison to its two congeners in Lake Biwa, Japan. ment of Pseudobagrus ichikawai (Siluriformes: Environ. Biol. Fish., 78, 135-146. Bagridae). Japan. J. Ichthyol., 41, 243-251. Maehata, M., Y. Nagata, M. Matsuda, H. Akiyama and Y. Yamane, H., T. Yokoyama, Y. Nagata and T. Yamada (2004) Tomoda (1990) Reproductive behavior of the Biwa- Reproductive ecology and early life history of the sheatfish, Parasilurus biwaensis. Japan. J. Ichthyol., 37, bagrid catfish, Pseudobagrus nudiceps. Japan. J. 308-313 (in Japanese with English abstract). Ichthyol., 51, 135-147 (in Japanese with English Matsuo, T. and H. Takahama (2004) Mating behavior of abstract). the freshwater catfish Pseudobagrus nudiceps Ageand growth of Liobagrus reinii 415

筑後川水系川原川におけるアカザの年齢と成長

竹下直彦・阪田和弘・近藤卓哉・永田新悟・荒木 晶・星野和夫

筑後川水系川原川産アカザの年齢と成長を明らかにすることを目的として，2000年 4 -12月に289個 体を採集した。本種の第 6 椎体には不透明帯と透明帯が交互に観察され，透明帯から不透明帯への境 界を標示とした。その標示は毎年 6 月に形成された。また，繁殖期は 5 - 7 月で，6 月がその盛期と考 えられた。本河川のアカザにおいては，体長の雌雄差が認められなかったことから，雌雄とりまとめ て，年齢と体長を von Bertalanffy の成長式にあてはめたところ，以下の式が得られた。

Lt = 127.4[1-exp{-0.434(t+0.537)}] （Lt：t 歳時の体長） この成長式より，満 1 歳で62.0 mm，2 歳で85.0 mm，3 歳で100.0 mmに達すると推定された。