Japan. J. Ichthyol. 魚 類 学 雑 誌 41 (1): 15-22, 19 94 41 (1): 15-22, 1 9 94

Growth, Maturity and Population Structure of the Bagrid , Pseudobagrus ichikawai, in the Tagiri River, Mie Prefecture, Japan

Katsutoshi Watanabe Laboratory of Ichthyology,Tokyo Universityof Fisheries, 4-5-7 Konan, Minato-ku,Tokyo 108,Japan

(ReceivedJune 16, 1993; in revisedform January 4, 1994;accepted February 22, 1994)

Abstract A smallpopulation of the bagrid catfish,Pseudobagrus ichikawai, was investigatedduring the period from April 1988to December 1989in the Tagiri River, Mie Prefecture,Japan. The catfish were nocturnally active from springto autumn, especiallyfrom June to September. During the daytime and in winter, they hid in crevicesalong the vegetatedriver shores or under boulders on the river bed. Analyses of seasonalchanges in size distributionand growth patterns of 202 individualsrevealed that the fish grew mainly in summer. New recruits, which appeared first in autumn, attained about 40 mm in standard length (SL) by July of the followingyear. At age 2 years, some femalesexceeded 60mm SL, being mature, whereasmales probably mature at 3 years, reaching about 100mmSL. The maximumsizes recorded were 93.5mm SL for femalesand 108.0mmSL for males. Sexualsize dimorphismwas apparent in immature, 1 year-old, becoming pronounced in older fish. The sex ratio of adults was largely female-biased. Although it appeared that spawningtook place in July of both years, no recruits representingthe 1988 year-classwere captured. Differencesoccurred between 1988and 1989in growth rates, maturation of 2- year-old females,and population structure. The possibilityof the having a polygynousmating system, with the populationsize and age structure being unstable owingto floods,is suggested.

The bagrid catfish fauna of Japan is represented by and abundance of the species, largely due to intense Pseudobagrus aurantiacus (according to Ueno [1974, human impact (Nagoshi, 1983). 1985], this species probably comprises two different This study was aimed at clarifying the life history species), P. ichikawai (= ichikawai), of this rare catfish, P. ichikawai, especially its

and nudiceps (Miyadi et al., 1976; growth, maturity and population structure. Mark- Sawada, 1984). The distributions of the species are recapture methods were used with the permission of geographically separated, with each species being the Japanese National Agency for Cultural Affairs. closely related to species in Korea and/or China (Nakamura, 1963; Ueno, 1985; Watanabe et al., 1992). Pseudobagrus ichikawai () is found Materials and Methods only in the rivers flowing into the Ise and Mikawa bays (Okada and Kubota, 1957; Nakamura, 1963). Study area The life histories of the Japanese bagrid have not been studied in detail, with only a few This investigation was conducted in the Tagiri reports on limited aspects of their ecology, e.g., the River (14 km long), Mie Prefecture, Honshu, Japan

early life history of P. aurantiacus (Okada and Sei- (35•‹10'N, 136•‹31'E). The river rises from the Yoro ishi, 1938). P. ichikawai has been observed inhabit- Mountains, flowing into the Inabe River. In the ing pools in the middle to upper reaches of rivers, middle and lower courses, it is a Bb-type river (Kani, remaining hidden under rocks by day, but actively 1971), 5-20 m wide. Weirs built approximately feeding on aquatic at night (Shimizu and every 200-300 m, have prevented upstream move- Shimizu, 1982; Shimizu, 1988). In 1977,P. ichikawai ment of fish at normal water levels. was designated as a "natural monument" for preser- Shimizu and Mori (1985) found Pseudobagrus vation purposes, owing to the rapid decline in habitat ichikawai only in the lower reaches (about 2km) of

•\ 15•\ K. Watanabe the Tagiri River. A section including the backwater comm.). The rate of disappearance of the injected of a weir in the lower reaches was selected for the latex, based on recaptured specimens with a notched main part of this study, owing to a preliminary adipose fin, was estimated to be less than 2%. survey which showed the density of the species in ales larger than 50mm SL were identifiablem by that area to be relatively high. The study site, about the prominent genital papilla posterior to the anus. 80m long and 10-18m wide (about 1000m2 in sur- The smaller fish were grouped together, because of face area), was separated from other habitats of P. the difficulty of determining their sex in the field. ichikawai by a weir of 80cm height at the lower end The age of eachmarked fish was estimated at the and rapids about 100m long at the upper end. The time of capture as follows: 1) when the size distribu- greatest water depth was 60-80cm at normal water tion was apparently polymodal, the age of a fish was levels. The river bed wasmostly covered with peb- determined by considering eachmode to represent an bles, along with some boulders and concrete blocks age group; 2) if age groups could not be determined with the banks comprising a complexmix of boulders from the size distribution, a fish was considered to be and dense vegetation, but not being protected by the same age as similar length (SL) fish of known concrete. Although the velocity of the surface current age. Spawning season and individual yearly growth at the center of the river was ordinarily about were also taken into consideration. Age was taken as 30cm/sec, flow along the shores was negligible. A the number of winter seasons experienced. detailed description of the area was given by Wata- The condition factor (CF) is used herein as the nabe (1990). index of femalematurity, being calculated as follows: [ Body weight (g) Methods CF= •~1000. {Body length (cm)}3]

mark-recapture investigations were carried out Locomotor activity (expressed as an activity one to three times amonth (2-7 days each) from index) was indicated by themean number of fish

April 1988 to December 1989. captured per hour during night investigations. During the day, Pseudobagrus ichikawai hiding under boulders were caught by hand net following removal of the latter. At night, fish swimming Results actively, but not quickly, were sought by flashlight and similarly captured. Search and capture efforts Diurnal and seasonal changes in activity were kept as consistent as possible. Column net- traps (30cm diameter by 80cm long) were baited From April to October, Pseudobagrus ichikawai with earthworms or fishing paste and set near boul- individuals were observed swimming in the open at ders along the shores from April to July, 1989. nighttime only, with no obvious fluctuations in noc-

Standard length (SL) and body weight (BW), turnal activity. During the daytime, only a few measured to the nearest 0.5mm and 0.1g, respective- catfish were found under boulders which could be ly, sex, external characters, and capture location moved by hand. By contrast, under and around a were recorded for all fish collected. Subsequently, concrete block of about 2m length and around crev- the fish weremarked, kept in a container for one or ices among shore vegetation, groups of 10-15 indi- more hours, and then returned to the river near their viduals were observed even in the daytime, during capture point. As a commonmark, a small V-shaped the summer season. notch was cut in the adipose fin of each fish. Al- Seasonal changes in locomotor activity of the though the notch could be recognized throughout catfish under study are shown in Figure 1. Relatively the study period, it was re-cut at each recapture for high activity was observed from June to September, easier recognition. From June 1988 to August 1989, when the water temperature was above 15•Ž. No all fish larger than 50mm SL, 142 females and 60 catfish were observed from November tomarch males, were also individuallymarked by the injection (water temperature below 10•Ž). of red or blue liquid latex by hypodermic syringe at two points on the body sides. The influence of latex Growth injection on survival and growth rates has been shown to be negligible (Riley, 1966; Yusa, pers. Total numbers of fishmarked are shown by sex

•\1 6•\ Life History of Pseudobagrus ichikawai

Fig. 1. Seasonal changes in locomotor activity of Pseudobagrus ichikawai, in the Tagiri River at night. See section of Methods for explanation of activity index.

and year-class in Table 1. Recapture ratios of in 1988 and 1989. marked fish in samples attained 80% in the 1987 For the older year-classes, age-2 groups could be year-class and 70% in older year-classes in the inves- recognized from the size distribution between April tigations in June 1989 and subsequently. and July in both 1988 and 1989, individuals reaching

Seasonal changes in size distribution of captured ca. 60mm SL (females) and 75mm (males) in July fish, and growth patterns of marked fish are shown (Fig. 2). A mode in the size distribution, comprising by sex in Figure 2. Individual growth patterns are larger fish, was considered to represent age 3 and given only for those individuals recaptured relatively older fishes. A few larger females were apparently often. referable to age-4 or older.

In 1988, fish measuring ca. 30mm SL in April Based on the age determined for each marked growing to ca. 50mm in August could not be sexed, individual, the size (SL) of each year-class in early and were recognized as belonging to the age-1 group July was calculated for both years (Table 2).

(1987 year-class). Fish of the 1989 year-class were Annual growth of females averaged about 10mm SL first captured on September 12, 1989 (range: 20.5 at age 2, but less than 10mm SL in older age groups.

28.8mm SL; mean•}SD: 24.8•}3.9mm, n=5).- Annual growth of males was higher, about 25-35

However, no fish of the 1988 year-class were found mm SL for the age-2 group, with the result that

during age 3, they exceeded 100mm SL. Thus, the

maximum size recorded in males (108.0mm SL) was Table 1. Total numbers of individually marked greater than that in females (93.5mm SL) (Fig. 2, Pseudobagrus ichikawai Table 2). On September 18, 1988, at which time the

sex of age-1 fish could be first identified, males (56.3

4.3mm SL, n=8) were already larger than •}fem-

ales (52.3•}2.9mm SL, n = 10) (t-test, one tailed, t=

2.41, df=16,p<0.05). Rapid growth occurred from

June to September, but rates decreased during the

•\1 7•\ K. Watanabe

(a) (b) Fig. 2. Seasonal changes in size distribution (upper) and growth of marked individuals (lower) for female (a) and male (b) of Pseudobagrus ichikawai in the Tagiri River. Shaded area: sex undetermined. winter (Fig. 2). The same was true in age-2 and older males (Fig. 3; The mean standard length of the age-2 fish in 1989 Kruskal-Wallis test, 1988: H=4.98, df=7, p>0.5; was significantly shorter than in corresponding fish 1989: H=13.03, df= 10, p>0.2). in 1988 for each sex (Table 2; female: t-test, one In age-2 and older females, however, seasonal tailed, t=3.83, df=11, p<0.01, male: t=2.96, df= changes were clearly recognized (Fig. 3; Kruskal- 8, p<0.01). Wallis test, 1988: H=97.62, df=6, p<0.001; 1989: H=101.78, df=10,p<0.001). The condition factor Spawning season and age at first maturity in these females increased from June to early July and sharply decreased around the middle of July to Seasonal changes in the mean condition factor August. Since the fluctuation was accompanied by were not significant in age-1 fish, irrespective of sex expansion and subsequent contraction of the abdo- (Kruskal-Wallis test, 1988: H=6.50, df=7, p>0.3). men, it was considered to be caused by gravidity and

Table 2. Mean standard lengths (mm) of Pseudobagrus ichikawai in early July

Numerals in parentheses: range, number of individuals. The highest age-group for each sex in each year includes all older fish. a Includes both sexes; b no recruitment; e t-test, one-tailed, p<0.01.

•\1 8•\ Life History of Pseudobagrus ichikawai

Fig. 3. Seasonal changes in the mean condition factor (CF) of Pseudobagrus ichikawai in the Tagiri River for each sex of age-2 and older fish. Vertical lines indicate standard deviation.

spawning, the latter taking place mainly in July. In the two years (Fisher's exact test, p < 0.01). fact, on July 22, 1989, a relatively large age-2 fish During the summer season, age-3 and older males

(63.0mm SL) released about 120 adhesive eggs (>ca. 90mm SL) had a darker body color and during handling (2.3•}0.2mm, longest egg diameter, swollen muscles about the head and nape. These

2.0•}0.1mm, shortest; n=10). appeared to be sexual characters, indicating that

Although all age-3 and older females underwent males attained maturity in their third year, one year abdominal swelling owing to gravidity, only a por- later than females. tion of the age-2 females did so. The proportion of such age-2 females was 73% (8/11) in 1988 and 6% Sex ratio

(2/32) in 1989, indicating a highly significant differ- ence in the proportion of sexually mature females in Of the catfish captured by hand net, female num-

Table 3. Sex ratios in age-2 and older Pseudobagrus ichikawai collected with different sampling methods

* p<0 .05; ** p<0.01 (Female>Male).

•\1 9•\ K. Watanabe

bers exceeded those of males in both overall total Although the age-1 group had a sex ratio of about

(female/male=4.8 in 1988 and 3.2 in 1989) and in all 1: 1 in 1988, a larger number of females than males months in which more than 20 individuals were were captured of fish older than age 1 (1988) or 2 captured (chi-squared test, one tailed, p<0.01, (1989). This sex ratio bias could be attributed to except in June 1988, p<0.05) (Table 3). either actual bias and/or sampling error resulting

Considered separately, age-2 and older females from the capture method. The smaller bias in the sex also outnumbered the corresponding male groups in ratio of trapped fish compared with that of fish 1988 (age-2: female/male=4.1, p<0.01; older: 5.2, captured by hand net suggests some behavioral dif- p<0.01), although in 1989, the sex ratio bias in age- ference between the sexes, e.g., older males captured 2 fish (1987 year-class) was insignificant (female/ less often by hand net, possibly because of their male =1.3, p>0.1) (Table 3). The sex ratio of the lower activity outside shelters. Nevertheless, because

1987 year-class showed no significant bias neither at the total number of males marked was also much 1 year old in 1988 (September 3-4: female/male= lower than that of females (Table 1), it can be

0.8, p>0.1; September 18: 1.3, p>0.1), nor in the concluded that more females actually existed than total number of marked individuals (female/male= males, suggesting either a higher mortality rate or

0.8, p>0.1, Table 1). emigration of males. If the morphological changes in For the trapped fish, the sex ratio bias for the males at age 3 were a true indication of their sexual overall total was insignificant (female/male=1.4,p> maturity, the sex ratio bias in mature fish overall, is

0.1), in contrast with those caught by hand net. even greater, due to the delayed maturation of males.

Only in the age-3 and older group, was the propor- Although breeding details of this catfish remain tion of females to males higher (female/male=1.8, unclear, the sexual size dimorphism, which results p<0.05), but the bias was smaller than in the case of from the faster growth and longer growth period of fish captured by hand net (chi-squared test, one the males, suggests the existence of a polygynous tailed, p<0.01). mating system in this species (Clutton-Brock and Harvey, 1984; Kozlowski, 1989), such being support- ed by the sex ratio bias in mature fish. Competition Discussion among males for reproductive resources likely exists, with the shelter being considered as a most important Growth, sex ratio and maturity resource, owing to spawning being carried out in that of the male (Watanabe, unpubl. data). The possibil- As have some previous observations (e.g., Shi- ity also exists that the sexual size dimorphism has mizu, 1988), this study indicated that Pseudobagrus resulted from female preference for larger males. In ichikawai is nocturnal, apparently feeding actively in a related species, Pseudobagrus fulvidraco, which is the open almost only at night, especially between widely distributed from Siberia to China, the larger

June and September (water temperature >15•Ž). males make burrows for spawning and subsequent During the day and other periods of inactivity (No- protection of the eggs and offspring (Nikol'skii, vember to March), the species takes shelter, usually 1954). Further studies are necessary to elucidate the in crevices along the vegetated shore or under large reproductive ecology of P. ichikawai and its relatives. boulders on the river bed. Growth occurred exclu- sively during the active, summer period. Yearly changes

Sexual dimorphism in body size was clearly recog- nized, resulting mainly from the higher growth rate The growth rate, proportion of mature fish in age- in males, especially in summer at age 2, at which time 2 females, recruitment of yearlings and age composi- also, some females matured. The latter phenome- tion differed between 1988 and 1989. The lower non, however, cannot be held solely responsible for proportion of mature females at age 2 in 1989 (1987 the sexual size dimorphism, because males had al- year-class), probably resulted from lower growth ready become larger than females during their first rates in the year-class. On the other hand, recruits year. Other factors, such as physiological or behav- representing the 1988 year-class were not caught ioral differences between sexes (e.g., feeding activi- from 1988 to 1989, even though breeding had obvi- ty), must also contribute to size dimorphism in this ously occurred in 1988. This might be attributable to species. the tremendous disturbance caused by three ty-

•\2 0•\ Life History of Pseudobagrus ichikawai phoons in July, August and September, 1988, and the J.R. Krebs and N.B. Davies, eds. Behavioural ecology: high frequency of changing river levels in May and an evolutionary approach, 2nd ed. Blackwell, Oxford. June, 1989. Kani, T. 1971. Ecology of the aquatic insects inhabiting a In a relatively stress-prone environment, such as a mountain stream. Pages 3-91 in Y. Makino, M. Tokuda and T. Shibutani, eds. The complete works of Tohkichi small stream, disturbances such as flooding strongly Kani, vol.1. Shisaku-sha, Tokyo. (In Japanese.) influence the population dynamics of some fish spe- Kozlowski, J. 1989. Sexual size dimorphism: a life history cies and assemblages (Schlosser, 1985; Matthews, perspective. Oikos, 54: 253-255. 1986). Differences in growth and recruitment be- Matthews, W.J. 1986. Fish faunal structure in an Ozark tween the two years of this study resulted in the size stream: stability, persistence and a catastrophic flood. (age) distribution being biased towards larger Copeia, 1986: 388-397. (older) fish in 1989 than in 1988. The population Miyadi, D., H. Kawanabe and N. Mizuno. 1976. Coloured structure of Pseudobagrus ichikawai in the study area illustrations of the freshwater fishes of Japan. Hoikusha, therefore seems prone to instability. It should also be Osaka. 462 pp.(In Japanese.) pointed out that the restricted distribution within Nagoshi, M. 1983. On the conservation of nekogigi. Iden, areas confined by the many weirs in the river accen- 37: 61-65. (In Japanese.) tuates the effects of naturally-changing conditions. Nakamura, M. 1963. Keys to the freshwater fishes of Japan fully illustrated in colors. Hokuryukan, Tokyo. 262 pp. (In Japanese.) Nikol'skii, G.V. 1954. Special ichthyology. (English Acknowledgments translation by J.I. Lengy and Z. Krauthamer, 1961. Israel Program for Scientific Translations, Jerusalem. I am very grateful to Prof. Makoto Nagoshi, Fac- 538 pp.) ulty of Science, Nara Women's University, and Dr. Okada, Y. and S. Kubota. 1957. Description of a new Seiichi Mori, Faculty of Science, Kyoto University, freshwater cat-fish Coreobagrus ichikawai, with an eme- for their invaluable advice, help, discussion and crit- ndation of the Coreobagrus Mori. Japan. J. Ichth- ical reading of the manuscript. Heartful thanks are yol., 5: 143-145. also extended to Prof. Akito Kawamura and Dr. Okada, Y. and R. Seiishi. 1938. Studies on the early life Hideo Sekiguchi, Faculty of Bioresources, Mie Uni- history of 9 species of fresh-water fishes of Japan. Bull. versity, who advised and assisted in the study, Mr. Biogeogr. Soc. Japan., 8: 223-253. Yoshitaka Shimizu, who provided invaluable infor- Riley, J.D. 1966. Liquid latex marking technique for small fish. J. Cons. perm. in Explor. Mer., 30: 354-357. mation and assisted in the field survey, and to Prof. Yasuhiko Taki, Dr. Hiroshi Kohno, Miss Ayaka (Japanese translation by T. Suzuki, 1970. News, Japan Sea Regional Fish. Res. Lab., [224]: 3.) Amaha and Mr. Neal M. Teitler, all of Tokyo Uni- Sawada, Y. 1984. Family . Page 59 in H. Masuda, versity of Fisheries, for their critical reading of the K. Amaoka, C. Araga, T. Uyeno and T. Yoshino, eds. manuscript. Assistance in the field survey by Mmes. The fishes of the Japanese Archipelago. English text. Taeko Kimura and Satoko Mizuno, and Messrs. Tokai Univ. Press, Tokyo. Shoichiro Yamamoto, Akihisa Sakai, Tomomi Schlosser, I.J. 1985. Flow regime, juvenile abundance, and Mizuno, Hitoshi Miyasaka and Yoshio Kawase is the assemblage structure of stream fishes. Ecology, 66: also greatly appreciated. The Board of Education of 1484-1490. Mie Prefecture and Hokusei Town, and the Shimizu, M. and Y. Shimizu. 1982. Researches on the fishermen's union of the Inabe River provided per- distribution of nekogigi and the environments of its mission and help for this research. The study was habitat in the Inabe River. Kansai Shizen-hogo-kikou Kaihou, (8): 13-24. (In Japanese.) partially supported by financial aid from the Board Shimizu, Y. 1988. Ecology and conservation of nekogigi. of Education of Mie Prefecture, the Kansai Organi- Tansuigyo-hogo, (1): 63-66. (In Japanese.) zation for Nature Conservation, and the TaKaRa Shimizu, Y. and S. Mori. 1985. Fish fauna and distribution Harmonist Fund. of the Inabe River in Mie Prefecture. Tansuigyo, (11): 135-142. (In Japanese.) Ueno, K. 1974. Chromosomal polymorphism and variant Literature Cited of isozymes in geographical populations of Pseudobagrus aurantiacus, Bagridae. Japan. J. Ichthyol., 21: 158-164. Clutton-Brock,T.H. and P.H. Harvey. 1984. Compara- (In Japanese with English abstract.) tive approach to investigatingadaptation. Pages 7-29 in Ueno, K. 1985. Karyotype of the Japanese and Korean

•\ 2 1•\ K. Watanabe

bagrid fishes. Kaiyo-kagaku, 17: 102-108. (In Japanese.) 弁 川 水 系)に 生 息 す るネ コギ ギ個 体 群 を 標識 採 捕 法 を 用 い て調 Watanabe, K. 1990. On an ecological research and conser- 査 した.本 種 は春 か ら秋,特 に6月 か ら9月 にか け て 夜間 に活 動 vation of the nekogigi, Coreobagrus ichikawai. Kansai し,日 中 や冬 期 に は 抽 水 植 物 の 繁 茂 す る 川 岸 部 の 横 穴 や 河 床 の Shizen-hogo-kikou Kaihou, 12: 49-56. (In Japanese.) 浮 石 の 下 に潜 ん で い た.体 長 分 布 の 季 節 変 化 と合 計202個 体 の Watanabe, K., S. Mori, M. Nagoshi, S.R. Jeon and Y. 標 識 魚 の 成 長 か ら,本 種 は主 と して夏 に 成 長 す る こ とが わ か っ た.秋 に最 初 に現 わ れ た 当才 魚 は翌 年 の7月 に は標 準体 長 約40 Shimizu. 1992. Morphological differences between two mmに 達 した.雌 の一 部 は2才 で体 長60mmを 超 え,成 熟 に 達 bagrid catfishes, Coreobagrus ichikawai and C. brevi- した.雄 は体 長 が約100mmに 達 す る3才 時 に成 熟 す る と推 測 さ corpus. Japan. J. Ichthyol., 39: 157-162. れ た.最 大 体 長 は雌93.5mm,雄108.0mmで あ っ た.未 成 熟 で あ る1才 時 に す で にサ イ ズ に お け る性 的 二 型 が 現 わ れ,高 齢 魚 で よ り顕 著 に な っ た.成 魚 の 性 比 は大 き く雌 に偏 って い た.両 年 と も産 卵 は7月 に 行 わ れ た と推 測 さ れ た が,1988年 級 群 にっ い て 田 切 川(三 重 県)に お け る ネ コ ギ ギPseudobagrus ichi- は全 く加 入 が 認 め られ な か っ た.本 種 が 一 夫 多 妻 的 婚 姻 形 態 を kawai(ナ マ ズ 目 ギ ギ 科)の 成 長,成 熟 お よ び 個 体 群 構 もっ 可 能 性,お よび 本 個 体 群 が 洪 水 な どに よ る撹 乱 に対 して不 造 安 定 で あ る こ とが 示 唆 され た. 渡 辺 勝 敏 (〒108東 京 都 港 区 港 南4-5-7東 京 水 産 大 学 魚 類 学 研 1988年4月 か ら1989年12月 の間,三 重 県 北部 の 田切 川(員 究 室)

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