Aquacult. Sci. 64（2），209－213（2016）
Note
Grey sea chub, Kyphosus bigibbus, is able to browse seaweed at night under rearing condition
1,＊ 2 3 Tsutomu NODA , Yasuhiro SHIMA , Kousuke YATSUYA , 1 4 Hirotaka MIZUOCHI and Taku YOSHIMURA
Abstract: The browsing ability of the grey sea chub, Kyphosus bigibbus, was examined under tank-rearing conditions. Ten fish (total length, 40.0-43.5 cm) were reared in each of two round 3 kl fish tanks. Brown seaweeds (Ecklonia kurome and Padina arborescens) were fed to the fish during different time periods (4:00-7:00, 11:00-14:00, 17:00-20:00 and 21:00-24:00). The average amount of seaweed browsed by the fish during the four periods ranged from 33.6 to 41.1 g/kg-fish/3-h for E. kurome and from 35.8 to 45.4 g/kg-fish/3-h for P. arborescens. The amounts of seaweed browsed were similar between the two species of seaweed and between the four time periods. These pre- liminary experiments suggest that K. bigibbus browses seaweed during any time period including night.
Key words: Kyphosus bigibbus, Herbivorous fish, Night browsing, Seaweed bed decline
In recent years, declines in areal extent of sea- sea chub Kyphosus bigibbus in particular grows weed beds have been observed in coastal areas to relatively large size and forms large schools of Japan, especially in southern Japan (Fujita (Kuwahara 2015). 2010; Vergés et al. 2014). One possible cause Yamaguchi et al. (2006, 2010) reported that for this decline is feeding pressure on macroal- K. bigibbus fed mainly on brown seaweed and gae by herbivorous fish (Kiriyama et al. 1999, showed relatively active migration during day- 2001; Kiyomoto et al. 2000; Fujita 2010; Vergés time in November. Our recent study of daily et al. 2014). Kiriyama et al. (2001) examined migration of K. bigibbus using bio-telemetry bite marks on seaweed and proposed that spe- systems showed their active migration during cies of sea chub (genus Kyphosus), the mottled night in spring. Welsh and Bellwood (2014) spinefoot Siganus fuscescens, and the Japanese reported diurnal and nocturnal movement of parrotfish Calotomus japonicus could have sig- the brassy chub Kyphosus vaigiensis at Orpheus nificant effects on the decrease in the seaweed Island in Australia, and implied a possibility of beds because of their active feeding on seaweed nocturnal feeding activity. However, any noc- in the coastal area of Nagasaki Prefecture. Grey turnal feeding on seaweed by Kyphosus species
Received 26 March 2015; Accepted 17 December 2015. 1 Goto Laboratory, Seikai National Fisheries Research Institute, Fisheries Research Agency, 122-7 Nunoura, Tamanoura, Goto, Nagasaki 853-0508, Japan. 2 Minami-Izu Laboratory, National Research Institute of Aquaculture, Fisheries Research Agency, 183-2 Minami-Izu, Kamo, Shizuoka 415-0156, Japan. 3 Miyako Laboratory, Tohoku National Fisheries Research Institute, Fisheries Research Agency, 4-9-1 Sakiyama, Miyako, Iwate 027-0097, Japan. 4 Seikai National Fisheries Research Institute, Fisheries Research Agency, 1551-8 Taira, Nagasaki, Nagasaki 851-2213, Japan. ＊Corresponding author: Tel, (+81) 959-88-2750; Fax, (+81) 959-88-2170; E-mail, [email protected] (T. Noda). 210 T. Noda, Y. Shima, K. Yatsuya, H. Mizuochi and T. Yoshimura has not yet been confirmed nor demonstrated. compare the amount of seaweed browsed over a Therefore, to clarify whether K. bigibbus specific time period by fish with an empty stom- browses seaweed during the night, the brows- ach, no food was supplied 21-24 h before each ing ability of the fish during different time peri- browsing experiment. ods was examined in a rearing tank. Previous studies showed that K. bigibbus browsed Sargassum species and Ecklonia Materials and Methods kurome (Inoue 2006; Yamaguchi et al. 2010; Yatsuya et al. 2012). Moreover, Yatsuya et al. Fifty K. bigibbus (total length, 35.5-49.0 cm) (2012) reported that seaweeds such as P. arbo- were caught by a set-net at Fukue Island in rescens and Zonaria diesingiana were domi- Nagasaki Prefecture, Japan, on 2 and 9 July nant in stomachs of K. bigibbus in August and 2013 and transferred to a floating net cage (4 m September. These studies indicate that K. bigib- square and 4 m deep) off Goto Laboratory bus can feed on diverse brown seaweed species. (Seikai National Fisheries Research Institute, The fish pre-reared in the floating net cage in Nagasaki Prefecture, Japan). The fish were this study fed well on both P. arborescens and S. fed two species of brown seaweed, Padina patens, which were dominant in the sea adjacent arborescens and Sargassum patens, collected at to Goto Laboratory. Because S. patens lost most Fukue Island. These seaweeds were bundled of its frond after maturation until August, in the and placed at the bottom of the cage with a main experiments from August to September stone weight. the fish were fed E. kurome obtained at Nagoya Ten similar-sized fish (total length, 40.0- Bay in Oita Prefecture and P. arborescens 43.5 cm) with no obvious signs of physical obtained at Fukue Island. damage were transferred to each of two round The seaweeds were stocked after collection fiberglass-reinforced plastic fish tanks (capacity, in a refrigerated chamber (5°C) for 1 to 6 days 3 kl; diameter, 2.4 m; depth, 0.8 m) on 16 and 23 before each experiment. Preweighed seaweed July. Sand-filtered seawater was supplied to the (about 1,100 g wet-weight) was fed at the start two tanks at 2 kl/h and water depth was main- of each time period, defined as period I (4:00- tained at 0.7 m. The mean (±SD) total length, 7:00), II (11:00-14:00), III (17:00-20:00) and fork length, and body weight of the fish were IV (21:00-24:00, Japan Standard Time). At the 42.0 ± 1.0 cm, 38.5 ± 0.8 cm, and 1.30 ± 0.15 end of each period, all un-browsed and scat- kg, respectively, in tank 1 and 41.4 ± 1.4 cm, tered seaweed left in the tank was collected and 38.2 ± 1.2 cm, and 1.27 ± 0.17 kg, respectively, weighed. The amount of browsed seaweed was in tank 2. There were no significant differ- calculated as the weight difference between ences between tanks in the lengths or weights the seaweed supplied and that remaining, of the fish (t-test, P > 0.05). Both tanks were and that amount was divided by the total wet- set outside away from any artificial light and weight of the fish in a tank and expressed as g/ covered during the whole day with a sheet of kg-fish/3-h. shade cloth (#1013; Earth Corporation, Tokyo, The experiments were repeated three times Japan; 85-90% light attenuation). The fish in for each seaweed species and each time period the tanks were fed P. arborescens during the using the same group of K. bigibbus. Different rearing period except on the day of a browsing fish were not used for each experiment because experiment. it would have been difficult to catch a sufficient Browsing experiments focusing on the noc- number of K. bigibbus of similar size with no turnal feeding ability of the fish were performed obvious signs of physical damage. One fish died from 6 August to 20 September 2013, although on 13 September and the total weight of fish in the experiment for period IV (described below) tank 2 dropped to 11.4 kg. No replacement fish was to be avoided on the night of a bright moon was introduced to avoid mixing of fish that had (Table 1). Because this study was designed to been reared under different conditions. After a Kyphosus bigibbus can browse seaweed during night 211
Table 1. Summary data for Kyphosus bigibbus seaweed browsing experiments Browsed seaweed Time Date (2013) Temperature (°C) Tank Seaweed (g/fish in tank/3-h) period number 1st exp. 2nd exp. 3rd exp. 1st exp. 2nd exp. 3rd exp. 1st exp. 2nd exp. 3rd exp. 1 490 525 705 I 10 Aug. 18 Sep. 20 Sep. 28.9 27.1 27.2 2 465 300＊ 400＊ 1 425 400 465 II 6 Aug. 12 Aug. 10 Sep. 28.0 28.8 27.1 Ecklonia 2 420 450 425 kurome 1 580 395 620 III 7 Aug. 12 Sep. 15 Sep. 28.2 27.4 27.6 2 505 575 445＊ 1 470 580 635 IV 8 Aug. 13 Sep. 16 Sep. 28.2 27.5 27.4 2 370 330 305＊ 1 650 620 410 I 17 Aug. 24 Aug. 8 Sep. 29.5 28.9 27.1 2 700 690 420 1 380 525 495 II 13 Aug. 20 Aug. 3 Sep. 28.8 29.6 27.9 Padina 2 415 580 360 arborescens 1 555 710 510 III 14 Aug. 21 Aug. 4 Sep. 28.9 30.1 27.3 2 440 700 495 1 505 600 470 IV 15 Aug. 22 Aug. 31 Aug. 29.1 29.0 29.7 2 535 555 395 The feeding experiment was repeated three times for each time period. Sunrise times ranged between 5:44 and 6:11, sunset times ranged between 18:31 and 19:18 during browsing experiments. ＊One dead fish was removed from tank 2 on 13 September, no replacement fish was added.
Shapiro-Wilk normality test, two-way repeated 60 E. kurome measures ANOVA was used to compare differ- ences in the amount of seaweed consumed for 40 each tank, seaweed, and time period. 20 Photon flux density (PFD) in the tanks was (g/kg-fish/3-h) Amount of browsd seaweed of browsd Amount measured on 15 September (no cloud cover 0 I II III IV P. arborescens Tank 1 and moon age of 9.6 days) with an underwater 60 (4:00–7:00) (11:00–14:00) (17:00–20:00) (21:00–24:00) Tank 2 quantum sensor (LI-192SA; Li-Cor, Inc., Lincoln, Time period Nebraska, USA) connected to a data logger (LI- 40 1400, Li-Cor). The detection limit was a PFD of
(g/kg-fish/3-h) 20 0.001 μmol/m2/s. PFD was measured every 5 Amount of browsd seaweed of browsd Amount minutes for each time period. 0 I II III IV On 24 October, daytime feeding behavior (4:00–7:00) (11:00–14:00) (17:00–20:00) (21:00–24:00) was recorded by a waterproof digital camera Time period (DMC-FT5; Panasonic, Osaka, Japan) and a video camera (HDR-SR1; Sony, Tokyo, Japan) in Fig. 1. Amount of seaweed (Ecklonia kurome (top) and a waterproof case, and night feeding behavior Padina arborescens (bottom)) browsed by Kyphosus bi- gibbus during each 3-h period. The amount of browsed was recorded by the video camera using a lamp seaweed was divided by the total wet-weight of the fish in with a near-infrared filter. a tank and expressed as g/kg-fish/3-h. Columns and error bars indicates means and standard deviations, respectively. Results and Discussion
Kyphosus bigibbus browsed both seaweeds of seaweed (n = 3, P > 0.05), and between the during all periods (Fig. 1). The amounts of four time periods (n = 3, P > 0.05, Fig. 1). The browsed seaweed were similar between the two PFD in the two tanks was below the detection tanks (n = 3, P > 0.05), between the two species limit during period IV on 15 September (Fig. 2). 212 T. Noda, Y. Shima, K. Yatsuya, H. Mizuochi and T. Yoshimura
Figure 3 shows typical browsing behavior of Though our experiments, including observa- K. bigibbus during both day and night on 24 tions by video camera, indicate that K. bigibbus October. Any noticeable difference between has the ability to detect and browse seaweed daytime and nocturnal feeding behavior was even in night, we cannot deny the possibility not observed. The night feeding observa- that the experimental fish with an empty stom- tions showed that K. bigibbus approaches sea- ach stumbled and fed on seaweed in the rearing weed slowly and browses seaweed definitely. tanks or that they fed on the seaweed in a blind Incidental or blind feeding was not observed way caused by the starvation at the begin- during night. ning of the experiment. Thus, more studies Because the experimental fish tanks were are needed to understand any diurnal feeding covered by a shade cloth that blocked 85-90% rhythms by conducting continuous browsing of light, the PFD was below 0.001 μmol/m2/ experiments over a day or a few days. In addi- s, even on a relatively bright night during the tion, further studies are needed to evaluate the experiments (moon age of 9.6 days). The light vision level of K. bigibbus or the possible use of condition in the tanks could be considered senses other than eyesight for finding seaweed. nearly dark at night during the experiments. Our preliminary study indicates that noctur- Our results suggest that K. bigibbus has both nal feeding by K. bigibbus should be taken into diurnal and nocturnal feeding ability. This is consideration for understanding the seasonal the first report of nocturnal feeding of herbiv- changes in amount of seaweed browsed, sea- orous fish in the genus Kyphosus under dark weed selectivity, and the impacts of browsing on conditions. seaweed beds.
Acknowledgments 100
80 The authors thank the staff of the Nagoya Tank 1 ）
/s Moba Conservation Association for their coop- 2 60 Tank 2 eration in collecting E. kurome in Nagoya Bay. μmol/m
（ 40 We are grateful to Mr. Yasumasa Yamamoto, PFD 20 a camera operator of NHK Nagasaki, for the night camera observations. We thank Dr. 0 0:00 3:00 6:00 9:00 12:00 15:00 18:00 21:00 0:00 Hideaki Aono, Mr. Yuichiro Fujinami, Mr. PeriodI PeriodII PeriodIII PeriodIV Setsuo Kiyomoto, Dr. Masahiro Nakagawa, Mr. Time of day Takurou Hotta, Mr. Kazunori Yoshida, and Dr. Fig. 2. Time series of photon flux density (PFD) in the Tatsuru Kadota of the Seikai National Fisheries two experimental tanks on 15 September 2013. Research Institute, for valuable comments
A B
Fig. 3. Photographs showing Kyphosus bigibbus browsing on seaweed during daytime (A) and night (B) on 24 October 2013. A light source with near-infrared filter was used for the night photograph. Kyphosus bigibbus can browse seaweed during night 213 on the manuscript. We deeply appreciate Mr. Japanese with English abstract). Hitoshi Shikuwa, Ms. Miyo Nagao, Mr. Koji Kuwahara H. (2015) The evaluation of current status for grazing control techniques of herbivorous fish. Fish. Tanaka, Mr. Tsuyoshi Kakuta, Mr. Hiroshi Eng., 51, 253-257 (in Japanese with English abstract). Kakuta, and Ms. Satsuki Kawakami of Goto Vergés A., P. D. Steinberg, M. E. Hay, A. G. B. Poore, A. H. Laboratory for rearing K. bigibbus, and Mr. Campbell, E. Ballesteros, K. L. Heck, D. J. Booth, M. Katsutoshi Hiramatsu, a fisherman on Fukue A. Coleman, D. A. Feary, W. Figueira, T. Langlois, E. M. Marzinelli, T. Mizerek, P. J. Mumby, Y. Nakamura, Island, for catching the K. bigibbus used in this M. Roughan, E. V. Sebille, A. S. Gupta, D. A. Smale, study. F. Tomas, T. Wernberg and S. K. Wilson (2014) The tropicalization of temperate marine ecosystems: cli- References mate-mediated changes in herbivory and community phase shifts. Proceedings of the Royal Society B, 22, doi: 10.1098. Fujita D. (2010) Current status and problems of isoyake in Welsh J. Q. and D. R. Bellwood (2014) Herbivorous fishes, Japan. Bull. Fish. Res. Agen., 32, 33-42. ecosystem function and mobile links on coral reefs. Inoue K. (2006) Growth and feeding ecology of the grey Coral Reefs, 33, 303-311. sea chub, Kyphosus bigibbus. Unpublished Master's Yamaguchi A., K. Inoue, K. Furumitsu, T. Kiriyama, T. Thesis, Nagasaki University, pp. 111. Yoshimura, T. Koido and H. Nakata (2006) Behavior Kiriyama T., A. Fujii, T. Yoshimura, S. Kiyomoto and and migration of rabbitfish Siganus fuscescens and T. Yotsui (1999) Leaf-lost phenomenon observed grey seachub Kyphosus bigibbus off Nomozaki, on three Laminariaceous species in coastal waters Kyushu, tracked by biotelemetry method. Nippon around Nagasaki prefecture in autumn 1998. Suisan Gakkaishi, 72, 1046-1056 (in Japanese with Aquaculture Sci., 47, 319-323 (in Japanese with English abstract). English abstract). Yamaguchi A., K. Furumitsu, N. Yagishita and G. Kume Kiriyama T., M. Noda and A. Fujii (2001) Grazing and bite (2010) Biology of herbivorous fish in the coastal marks on Ecklonia kurome, caused by several herbivo- area of western Japan. Coastal Environmental and rous fishes. Aquaculture Sci., 49, 431-438 (in Japanese Ecosystem Issues of the East China Sea, pp. 181-190. with English abstract). Yatsuya K., S. Kiyomoto and T. Yoshimura (2012) Seasonal Kiyomoto S., T. Yoshimura and S. Arai (2000) Grazing changes of stomach contents of herbivorous fish selectivity of herbivorous fishes on five macroalgae Kyphosus bigibbus in sub-tropical seaweed bed. Algal in sublittoral zone at Nomozaki, Nagasaki prefec- Resources, 5, p. 28 (in Japanese). ture. Bull. Seikai Natl. Fish. Res. Insti., 78, 67-75 (in
飼育実験で観察されたノトイスズミの夜間摂餌
野田 勉1・島 康洋2・八谷光介3・水落裕貴1・吉村 拓4
ノトイスズミが海藻を摂餌可能な時間帯を明らかにする目的で，全長40.0 ～ 43.5 cm の本種を 3 kl 水槽 2 面に各10個体収容して水槽実験を行った。クロメおよびウミウチワを 4 つの時間（4:00， 11:00，17:00，21:00）ごとに与え，それぞれ 3 時間後に残った海藻を回収して摂餌量を算出し た。その結果，各時間帯の摂餌量は，クロメでは33.6 ～ 41.1 g/kg-fish/3-h，ウミウチワでは35.8 ～ 45.4 g/kg-fish/3-h で，時間帯間および海藻種間に有意差はなかった。また，夜間撮影の映像からは 昼夜の摂餌行動に顕著な差は認められなかった。以上の結果より，飼育条件下においてノトイスズミ は夜間を含む 4 つの時間帯いずれにおいても海藻を摂餌可能であることが示された。