First record of Acetes sibogae sibogae in Biogeography 19. 35–46. Sep. 20, 2017

Growth and early gonadal development in boreal Barbatula oreas (Jordan & Fowler, 1903) introduced into a temperate river in central , Japan

Rui Hatakeyama1, Tadashi Kitano2 and Yoshiyasu Machida3

1 Civil Engineering and Eco-Technology Consultants, 2-23-2 Higashiikebukuro, Toshima, Tokyo 170-0013, Japan 2 School of Humanities and Culture, Tokai University, 4-1-1 Kitakaname, Hiratsuka, Kanagawa 259-1292, Japan 3 Bihoro Museum, 253-4 Midori, Bihoro, District , 092-0002, Japan

Abstract. Growth and early gonadal development of boreal Barbatula oreas were investigated in invasive (Kaname River, central Honshu) and native (Komaoi River, northeast Hokkaido) populations in Japan. The relationship between growth and water temperature was compared in the two populations. The monthly mean water temperature changed seasonally between 7.6 and 21.1°C in the Kaname River and between 1.2 and 15.0°C in the Komaoi River. Age-0 fish in the Kaname River first appeared in April and reached 78.5 mm body length (BL) in the following March. Age-0 fish in the Komaoi River appeared in July, reached 48.4 mm BL in November, but remained at 50.8 mm BL in the following March, indicating stagnant growth during winter. The gonads of age-0 fish in the Kaname River had distinguishable ovaries and testes in November, un- like the gonads of fish in the Komaoi River, which were indistinguishable in all age-0 fish until the following February. Fast growth and gonadal development in B. oreas of the Kaname River is attributed to the environ- mental characteristics of the temperate river, which enables earlier spawning and allows the fish to remain longer at a temperature suitable for growth.

Key words: , alien species, temperature, length frequency, acclimatization

Introduction different life history traits from those in their natural range (Fox et al., 2007; Alp et al., 2011; Grabowska Establishment of alien fish often significantly in- et al., 2011; Ishikawa et al., 2013), and these altered creases the risk to native species through processes traits may have an impact on the ecosystem. such as competition, predation, and hybridization Water temperature greatly affects the growth rate (Ogutu-Ohwayo, 1990; Swift et al., 1993; Suzuki & of fish (Brett, 1979). Generally, within an optimal Kato, 1996; Maezono & Miyashita, 2003; Ling & temperature range, growth rate increases with water Willis, 2005). Alien fish experience a different and temperature, until the water exceeds this optimal new environment after artificial introduction into range, then growth decreases with increasing tem- a region outside their natural range. Alien fish that perature. In teleost fish, puberty is initiated depend- are successfully established in a new region express ing on body size (Okuzawa, 2002; Taranger et al., ——————————————————————— 2010). Therefore, differences in growth rate affect *Corresponding author: [email protected] the time to reach puberty.

− 35 − Growth of alien Barbatula oreas Rui Hatakeyama, Tadashi Kitano and Yoshiyasu Machida

The Barbatula Linck, 1790 is distributed growth pattern. from Northern Asia to Europe, and includes 18 spe- cies (Kottelat, 2012; Prokofiev, 2015). Barbatula Materials and methods oreas occurs naturally in Hokkaido, Japan, in the eastern end of the distributional region of the genus. Fish collection and temperature The distributional area of B. oreas has expanded Specimens were collected in the Kaname to lower latitudinal rivers, such as the (E139°13′36″N35°23′24″) located in cen- River, , , and tral Honshu, Japan and in the Komaoi River in northeastern Honshu, by the release of salmonid (E144°07′48.8″N43°49′11.2″, sys- seeds (Ministry of Land, Infrastructure, 2017). In tem) located in northeast Hokkaido, Japan. Sampling recent years, B. oreas has also been established in was conducted for 2 h once a month from April the upstream Kaname River flowing through central 2013 to March 2015 in the Kaname River and with Honshu (Yashima et al., 2011), the lowest latitude at no time limit from May 2014 to June 2015 in the which it is found as an invasive species. Komaoi River. During these periods, a data logger There is little ecological knowledge on the growth (UA-002-64: Onset Computer Co., USA) was placed and maturation of B. oreas in its natural and invasive in the water and temperature data were recorded ranges. Barbatula oreas possesses ecological traits, every hour. Fish were collected using a combination such as foraging for benthic invertebrates (Miyadi of an electric shocker (LR-20B: Smith-Root, USA) et al., 1963). This species tends to be the dominant and hand nets. In the Komaoi River from December species in its natural and invasive ranges (Toujo & 2014 to May 2015, fish were collected only using Hosoya, 1998; Nogami et al., 2001; Nagasawa et al., hand nets because they entered into thickets of 2009). In the Kaname River in the autumn of 2014, B. grass. Small fish were also collected using a hand oreas was the most dominant species by number and net. Fish collected in the Kaname River were anes- weight, accounting for approximately 50% of the thetized with MS-222 in a laboratory at the School total weight of fish (Hatakeyama & Kitano, unpub- of Humanities and Culture, Tokai University and lished data). subjected to body measurement. Fish in the Komaoi The Kaname River is a temperate river located River were anesthetized with clove oil (NOW Foods, in central Honshu, and its water temperature dif- USA) (Soto & Burhanuddin, 1995) immediately fers from that of the subarctic rivers in Hokkaido, after collection and fixed in 10% neutral formalin or in which B. oreas is naturally distributed. An un- 70% ethanol for later body measurement. derstanding of the biological mechanisms through which B. oreas acclimates and establishes itself in a Fish measurements temperate river is required to assess the ecological Body length (BL) and body weight (BW) of fish impact of this species on aquatic organisms. In this were measured. Gonads of fish <100 mm BL were study, body size growth was investigated in an in- removed and identified as ovary or testis under a vasive population in the Kaname River and a native stereomicroscope. Gonad weight (GW) was mea- population in Hokkaido, and the relationship be- sured and then used to calculate the index of gonadal tween growth and water temperature was compared growth, gonadosomatic index (GSI), as follows: GSI between the two populations. Early gonadal devel- = 100 × GW/BW. BL for specimens collected in the opment was also investigated with reference to the Komaoi River was corrected by a shrinkage factor

− 36 − Growth of alien Barbatula oreas Rui Hatakeyama, Tadashi Kitano and Yoshiyasu Machida

(10% neutral formalin: 0.96, 70% ethanol: 0.95), the Kaname River and May 5 in the Komaoi River. which was calculated using specimens from the Embryonic periods in are dependent on water Kaname River. temperature (Tompson & Riley, 1981; Nakajima et al., 2006). The period of B. oreas was 6.0 days at Data analysis 16.0°C (Hatakeyama & Kitano, unpublished data) For growth analysis, length frequency analysis and 1.6 days at 25.0°C (Kobayasi & Moriyama, was used because age characters of B. oreas in the 1957). The peak of hatching was defined as April Kaname River were obscure in calcified tissues such 13 in the Kaname River and May 15 in the Komaoi as the otolith and opercular bone. Length frequency River on the basis of the temperature-embryonic pe- for each sampling period was prepared in a 5.0-mm riod relationship and water temperature at the peak class width. Smoothing for each class was performed of spawning (12.4°C in the Kaname River, 9.7°C in with the previous and next class using a three-point the Komaoi River). The growth rate in each month moving average. Length frequency was divided was obtained from the growth formula. The monthly into a mixed normal distribution by the Hasselblad mean temperature in the Kaname River was obtained method, and the mean for each mode was calculated by averaging data for the two years that sampling (Aizawa & Takizawa, 1997). The Pauly and Ga- was conducted. The correlation between monthly schutz growth equation (Pauly & Gaschutz, 1979) growth rate and monthly mean temperature was de- was used to extend the von Bertalanffy equation by termined. To adjust for the developmental stage in adding variation of seasonal growth rate and was fit- the two rivers, data for growth rate were used in the ted to the means of modes and 3.7 mm BL at hatch- range from 35.0 to 110.0 mm BL. Growth differenc- ing (Hatakeyama & Kitano, unpublished data): es between males and females were not analyzed in

Lt = L∞ {1 - exp [-K (t/365 - t0) - (CK/2π) sin (2π detail. However, for some sampling dates, the BL

(t/365 - ts))]}, of males and females for each mode were evaluated

where Lt is the theoretical BL (mm) at age t (day); by the Steel-Dwass test. The relationship between

L∞ is the asymptotic BL (mm), C is the intensity of growth rate and water temperature was also evaluat- seasonal growth oscillations, K is the coefficient of ed by the Spearman rank correlation coefficient anal-

growth, t0 is the theoretical age (days) at Lt = 0, and ysis. The Mann-Whitney U test was used to test GSI

ts is the age at the beginning of growth oscillation. differences among sampling dates, and the Steel- These parameters were estimated by the maxi- Dwass test was used to determine GSI differences mum likelihood method (Gorie, 2001). Age was es- among ovaries and testes in a river or two rivers in timated as 0 days old at a peak of hatching. The peak the same month. was determined by adding an embryonic period to the date at the peak of spawning, which was indexed Results to the peak of GSI of female because GSI decreased rapidly to less than half of the peak one month later, Water temperature suggesting concentrated spawning in a short period. The daily mean water temperature in the Kaname As the peak of the GSI was between late March and River changed seasonally between 5.0 and 22.8°C middle April in the Kaname River and early May in from April 2013 to June 2015 (Fig. 1). The month- the Komaoi River (Hatakeyama et al., unpublished ly mean water temperature was highest in August data), the peak of spawning was set as April 5 in (21.0°C in 2013 and 21.1°C in 2014) and lowest

− 37 − Growth of alien Barbatula oreas Rui Hatakeyama, Tadashi Kitano and Yoshiyasu Machida in January (7.6°C in 2014 and 8.6°C in 2015) in 62.7 mm BL on September 1 (141 days old) of the each year. The daily mean water temperature in the hatching year and 78.5 mm BL on March 1 in the Komaoi River was between 0.1 and 16.8°C from following year (322 days old), but then showed May 2014 to May 2015 (Fig. 1). The monthly mean modest growth and only reached 111.0 mm BL on water temperature was highest at 15.0°C in August March 1 of the next year (687 days old) (Fig. 4). A and lowest at 1.2°C in January. The monthly mean large difference in growth by cohort was found in water temperature in the Kaname River was 4.4 to the Kaname River using the two-year data. The av- 7.9°C higher than that in the Komaoi River over the erage length of cohort 3 was 96.3 mm BL on March year. 15 (701 days old) and 99.1 mm BL on May 17 (764 days old), that is, <100 mm BL. Length frequency data Barbatula oreas in the Komaoi River reached The smallest length mode in the Kaname River 48.4 mm BL on November 1 (170 days old) of the first appeared in June 2013 (mean 35.8 mm BL, co- hatching year, but was only 50.8 mm BL (290 days hort 3), July 2014 (mean 54.8 mm BL, cohort 4), and old) on March 1 in the following year, indicating April 2015 (mean 12.5 mm BL, cohort 5) (Fig. 2). stagnant growth during winter (Fig. 5). Then, B. ore- The smallest mode in 2015 appeared earlier because as reached 91.3 mm BL on November 1 (535 days small larvae were found in a small pool in a river- old), but remained at 93.6 mm BL on March 1 of the bank. In contrast, the smallest mode in the Komaoi next year (655 days old). River first appeared in July 2014 (mean 36.2 mm There was no significant difference in BL between BL, cohort 3) (Fig. 3). In the Kaname River, fish <20 the sexes collected in January 2014, August 2014, mm BL appeared only in June in 2013 and in April and February 2015 in the Kaname River, or in May and May in 2015. Five cohorts were found through- 2014 and May 2015 in the Komaoi River (Table 1, out the sampling period. Cohort 3 included a large all P > 0.05). number of fish and appeared continuously from June 2013 to the end of the sampling period, whereas Growth rate and water temperature other cohorts were only present for limited periods. The growth rate of B. oreas in the Kaname River Three cohorts were found simultaneously in August was 0.01–0.35 mm/day and changed seasonally, with and November 2014 in the Kaname River and in Au- gust 2014 in the Komaoi River.

Growth Growth equations were determined by fitting to mean values for the cohorts obtained each month (Figs. 4, 5). Kaname River: Lt = 140.442{1 - exp [-0.743 (t/365 + 0.313) -(0.057/2π) sin (2π (t/365 - 5.240))]} Komaoi River: Lt = 1516.348{1 - exp [-0.030 (t/365 + 0.439) - (-0.004/2π) sin (2π (t/365 - Fig. 1. Seasonal variability in the daily mean water temperature 2.721))]} in the Kaname River (thick line) and the Komaoi River Barbatula oreas in the Kaname River reached (thin line).

− 38 − Growth of alien Barbatula oreas Rui Hatakeyama, Tadashi Kitano and Yoshiyasu Machida

Fig. 2. Length frequency of Barbatula oreas in the Kaname River. C1-C5: cohort 1-cohort 5.

− 39 − Growth of alien Barbatula oreas Rui Hatakeyama, Tadashi Kitano and Yoshiyasu Machida Fig.3.

300.3 May 12, 2014 Dec. 16 (n = 69) (n = 10) 200.2 C2 C3 100.1 C1 00 300.3 Jun 15 Jan. 12, 2015 (n = 54) (n = 11) 200.2 100.1 C1 00 300.3 Jul. 15 Feb. 11 (n = 36) (n = 0) 200.2 No data 100.1 C3 00 300.3 Aug. 14 Mar. 9 (n = 66) (n = 26) 200.2 100.1 00 300.3 Sep. 15 Apr. 11 (n = 74) (n = 40) 200.2 100.1 Relative frequency (％) 0 300.3 Oct. 9 May 9 (n = 45) (n = 69) 200.2 100.1 0 300.3 Nov. 12 5 50 100 (n = 40) 200.2 100.1 00 5 50 100 Body length (mm)

Fig. 3. Length frequency of Barbatula oreas in the Komaoi River. C1-C3: cohort 1-cohort 3.

Fig. 4. Mean body length at estimated age and growth curve Fig. 5. Mean body length at estimated age and growth curve for Barbatula oreas in the Kaname River. for Barbatula oreas in the Komaoi River.

− 40 − Growth of alien Barbatula oreas Rui Hatakeyama, Tadashi Kitano and Yoshiyasu Machida

a peak in June and the lowest rate in January (Fig. ture in each river (both P < 0.01) but the correlation 6). The peak in June decreased with age from 0.35 coefficient was higher in the Komaoi River (r = mm/day in age-0 fish to 0.16 mm/day in age-1 fish 0.967) than in the Kaname River (r = 0.730) (Fig. 7). and 0.08 mm/day in age-2 fish. The growth rate in age-0 fish was 2.10–4.67 times higher than that in Early gonadal development older fish. The growth rate in the Komaoi River was In the gonads of B. oreas yearling (cohort 3) in -0.02–0.26 mm/day and changed seasonally. The the Kaname River, it was possible to identify ovaries lowest rate at each age was lower than that in the and testes in November 2013 because ovaries were Kaname River. The peak in August did not decrease enlarged and had obvious oocytes. GSI in the ovary with age and was higher in age-1 and age-2 fish than increased from 5.0 ± 1.0 (mean ± SE) in November for those in the Kaname River. The monthly mean 2013 to 10.4 ± 2.1 in April 2014, although there was water temperatures during the sampling period were no significant difference among months (all com- 8.1–20.7°C in the Kaname River and 1.2–15.0°C in binations; P > 0.05) (Figs. 8). GSI did not change the Komaoi River. There was a significant positive significantly in the testis. GSIs were significantly correlation between growth rate and water tempera- different among males and females (all months; P < 0.01). Gonads of age-0 fish in the Komaoi River were stringy in shape and it was difficult to identify ovaries and testes under a stereo microscope in No- vember 2014. One and three ovaries were identified in five gonads in March and April 2015, respectively. GSI in the Komaoi River ranged from 0.18 ± 0.03 in November 2014 to 0.55 ± 0.15 in April 2015 but there was no significant difference among months (all combinations; P > 0.05) (Figs. 8). GSI was signifi- cantly lower for the gonad in the Komaoi River than that for the testis in the Kaname River (all months; P Fig. 6. Growth rate of Barbatula oreas in the Kaname River < 0.01) (Figs. 8). ( ＊ ) and the Komaoi River ( ◆ ).

Discussion

The growth rate of B. oreas in the Kaname River was 2.10–4.67 times higher in age-0 fish than in older fish. Age-0 fish reached approximately 79 mm BL by the following March, which is larger than the length in the Komaoi River, approximately 51 mm BL. The growth rate in older fish appeared to remain low because age-0 fish grew rapidly and reached a certain body size by the following spring. Fig. 7. Relationship between water temperature and growth rate of Barbatula oreas in the Kaname River ( ＊ ) and Barbatula oreas in the Komaoi River showed an the Komaoi River ( ◆ ). obvious stagnancy in growth during winter, with a

− 41 − Growth of alien Barbatula oreas Rui Hatakeyama, Tadashi Kitano and Yoshiyasu Machida

Figs. 8. Gonadosomatic index of yearling Barbatula oreas in the Kaname River. Numbers in the figures indicate the number of individuals. Asterisks indicate significantly different from each other (**: P < 0.01, *: P < 0.05). Asterisks in the upper figure indicate difference between ovary (●) and testis (○) in the Kaname River. Asterisks in the lower figure indicate difference between testis (○) in the Kaname River and gonad (ovary: ●, indistinguishable gonad: ◇ ) in the Komaoi River.

Table 1. Sex difference in body size of Barbatula oreas in the Kaname River and the Komaoi River. River Year Date Sex BL (mean ± SE) n Steel-Dwass test Age Kaname R. 2014 18 January Male 89.2 ± 4.3 14 + P ＞ 0.05 0 Female 80.5 ± 1.7 14 ( <115 mm BL) 16 August Male 98.9 ± 1.3 25 + P ＞ 0.05 1 Female 96.0 ± 1.3 25 ( >70 mm BL, <115 mm BL) 2015 21 February Male 107.9 ± 2.8 5 P ＞ 0.05 1+ Female 99.7 ± 2.4 13 Komaoi R. 2013 12 May Male 105.7±1.1 38 + P ＞ 0.05 1 Female 105.3±4.4 2 ( >75 mm BL) 2014 9 May Male 103.1 ± 1.0 25 + P ＞ 0.05 2 Female 91.8 ± 7.5 6 ( >75 mm BL) growth pattern that correlated strongly with water August was approximately 38 mm BL for age-0 fish temperature. In the closely related fish, B. toni (Dy- and 76 mm BL for age-1 fish in the Komaoi River, bowski, 1869), which inhabits Lake Kurazhechnoe and approximately 53 or 67 mm BL for age-0 fish in the Kamchatka Peninsula, two modes of 40 and and 92 mm BL for age-1 fish in the Kaname River. 80 mm in total length (TL), which, unlike BL, in- The smaller body sizes of B. toni and B. barbatula, cludes the length of the caudal fin, appear in August as well as B. oreas in the Komaoi River, show that (Tokranov, 2006). In B. barbatula (Linnaeus, 1758) growth is slower than that in B. oreas in the Kaname in the Lake District of the United Kingdom, two River. These findings suggest that the decrease in modes of 35–40 and 70 mm TL are found in August growth rate during winter is general in fishes of Bar- (Smyly, 1955). These seem to be age-0 fish in the batula distributed in high latitudinal regions. smaller mode and age-1 fish in the larger mode. In Yearling B. oreas in the Kaname River reached the present study, the average length of B. oreas in approximately 79 mm BL by the following March

− 42 − Growth of alien Barbatula oreas Rui Hatakeyama, Tadashi Kitano and Yoshiyasu Machida

and had more developed gonads, which could be initiate the spawning period (Okuzawa et al., 1989; clearly distinguished as testes and ovaries. These ob- Shimizu & Hanyu, 1991; Koya & Kamiya, 2000). B. servations were in contrast with yearling B. oreas in sawadai inhabiting the Baikal Lake system in east- the Komaoi River, which was approximately 51 mm ern Siberia spawn during May to June and the water BL in spring with string-like gonads. Thus, the high temperature is 6–12°C (Skryabin, 1993). Water tem- growth rates of B. oreas in the Kaname River aided perature in the Kaname River rises to this tempera- in attaining a body size that accompanied gonadal ture earlier than that in high latitudinal regions such development over a shorter period. as the Komaoi River and the Baikal Lake system. The lifespans of B. oreas in the Kaname and This may explain why spawning in the Kaname Riv- Komaoi Rivers are not clear. However, many in- er occurs earlier, leading to an earlier appearance of dividuals appear to live up to at least two years, as yearling fish. three cohorts were found simultaneously in these By spawning earlier and remaining for a longer rivers. The lifespan of the genus Barbatula is 3–5 period at a temperature suitable for growth, B. oreas years for B. barbatula in the United Kingdom (Smy- in the Kaname River can reach approximately 79 ly, 1955; Morris, 1963; Mills et al., 1983), 6 years mm BL by the following March, compared to the for B. barbatula in Finland (Sauvonsaari, 1971), and approximately 51 mm BL in the Komaoi River. Fast 8 years for B. sawadai (Prokofiev, 2007) in Eastern growth requires a large quantity of food, and B. ore- Siberia (Skryabin, 1993). It is a likely that the lifes- as in the Kaname River is thought to feed on more pan of B. oreas is shorter compared to these closely benthic , such as aquatic insects, than in the related species that inhabit high latitudinal rivers. Komaoi River. Native fish of 7 species belonging to In the present study, the peak period of hatching Cyprinidae, Cobitidae, Gobiidae, and Nemacheilidae in the two rivers, May in the Komaoi River and April inhabit the section of the Kaname River in which B. in the Kaname River, was estimated by the peak of oreas is established (Hatakeyama & Kitano, unpub- spawning, which was indexed to the peak of GSI of lished data), and all these species feed on benthic female. The smallest group in the Komaoi River was animals to some extent (Kawanabe, 1959; Mizuno, approximately 36 mm BL in July. A group with simi- 1961; Miyadi et al., 1963; Nakamura, 1969; Katano lar length (approximately 36 mm BL) in the Kaname et al., 2004; Kanou et al., 2007). Fast growth and River appeared in June. The earlier appearance of large number of B. oreas established in the temper- juveniles in the Kaname River corresponds to the es- ate Kaname River seem to be causing over competi- timated earlier peak of spawning or hatching. GSI in tion for food resources with native fish. In cohort 3 B. oreas rapidly decreases to 50% or less of the peak (2013 class), which had a large number of individu- after one month (Hatakeyama & Kitano, unpublished als, BL of age-2 was smaller; that is, growth was less data). Small fish were not collected in the Komaoi than that in cohort 1 and cohort 2. This suggests a River but fish <20 mm BL in the Kaname River were decrease in intense feeding by B. oreas on prey such only present during one or two months of the year. as benthic invertebrates. The peak of GSI is generally considered to be valid as an index of the peak of spawning. This seems to Acknowledgments be related to the relatively concentrated spawning in a brief period after the peak of GSI. We thank Zenkoh Hasegawa of the Bihoro Muse- In spring-spawning fishes, warm temperatures um for his help with collection of B.oreas. We also

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fish. Gen. Comp. Endocr., 165: 483-515. tulus toni (Dybowsky) from the Surikami River in Tokranov, A. M., 2006. Distribution and some fea- Fukushima City. Fukushima seibutsu, 41: 33-36. tures of the biology of the bearded stone loach Yashima, N., Tamino, T. & Kitano, T., 2011. Notes Barbatula toni (Balitoridae) in the Kamchatka of Pungtungia herzi and Noemancheilus barbat- river basin. J. Ichthyol., 46: 722-727. ulus toni as domestic alien species collected from Tompson, B. M. & Riley, J. D., 1981. Eggs and Kaname River. Nat. Hist. Rep. Kanagawa, 32: larval development studies in the north sea cod 109-113. (Gadus morhua L.). Rapp. P.-v. Réun. Cons. int. Explor. Mer., 178: 553-559. Toujo, K. & Hosoya, K., 1998. Noemacheilus barba- (Received June 30, 2017; Accepted September 8, 2017)

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