Growth and Early Gonadal Development in Boreal Barbatula Oreas (Jordan & Fowler, 1903) Introduced Into a Temperate River in Central Honshu, Japan
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First record of Acetes sibogae sibogae in Japan 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 Honshu, 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, Abashiri District Hokkaido, 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 fish 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: Nemacheilidae, 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 genus 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 Abukuma River (E139°13′36″N35°23′24″) located in cen- River, Agano River, Mogami River, and Kuji River tral Honshu, Japan and in the Komaoi River in northeastern Honshu, by the release of salmonid (E144°07′48.8″N43°49′11.2″, Abashiri River 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 fishes 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).