Biogeography 17. 13–20. Sep. 20, 2015

Horizontal and vertical distribution of reinii (Pisces: ) in Lake Biwa, central Japan

Yasuhiro Fujioka1,2*, Akihisa Sakai1 and Atsuhiko Ide1

1 Shiga Prefecture Fisheries Experiment Station, Hassaka 2138-3, Hikone, Shiga, Japan 2 Lake Biwa Museum, Oroshimo 1091, Kusatsu, Shiga, 525-0001 Japan

Abstract. The distribution of Utsusemi-kazika Cottus reinii in Lake Biwa was investigated by means of small trawl-net, commercial trawl-nets, and commercial set-nets. C. reinii were abundant in the coastal bot- tom waters deeper than 20 m between June and August and deeper than 30 m in October. These were mostly small of less than 4 cm SL, showing a mode in the 1-1.99 cm class in June. Fish of more than 4 cm SL also were caught in coastal waters (10-20 m in depth) and offshore deep waters (deeper than 40 m) throughout the year. These results suggest that this species leaves the plankton to begin its benthic life at a size of about 1 cm SL at depths of 20-30 m. After growing to 3-4 cm SL by October at depths of 30-40 m, they expand their range to bottom waters deeper than 40 m. The bottom sediment of the lake habitat is mainly fine mud, very different from the reported of gravel-bottom habitat of this fish in rivers.

Key words: Cottus reinii, Utsusemi-kazika, Distribution, Lake Biwa

Introduction is chiefly distributed in shallow coastal waters with stony bottoms and occasionally in muddy deep wa- The genus Cottus has a circumpolar distribution ters, and it spawns in rivers (Nakamura, 1975; Goto, in the northern hemisphere and includes more than 1995). Recently, this fish has been shown to inhabit 60 species of sculpin confined to freshwater (Berra, in the lower reaches of rivers flowing into the North 2001; Nelson, 2006; Yokoyama & Goto, 2011). Its Basin of Lake Biwa throughout the year (Fujioka et life cycle is commonly fluvial, but some species al., 2014). The distribution of C. pollux has never are amphidromous (Goto, 1994). In the freshwater been overlap with that of C. reinii. Its occurrence in drainages of the Japanese Archipelago, six species Lake Chuzenji in Tochigi Prefecture is due to unin- of Cottus are found (Nakabo, 2013). Among these, tentional introduction from Lake Biwa (Yokoyama C. pollux mainly inhabits upper reaches of rivers and & Yamamoto, 2012). C. reinii has an amphidromous lays comparatively few large eggs, while C. reinii life style, and its larvae are known to descend to the lives in the middle and lower reaches of rivers and lake and become bottom dwellers (Goto, 1995), but spawns many small eggs. The latter species compris- there has been no detailed study of its distribution es two types (small- and middle-egg types) (Nakabo, in the lake. Such knowledge is important in order to 2013). The small-egg type of C. reinii also lives in elucidate the life-history segregation of this species Lake Biwa and is known there as Utsusemi-kazika; and the evolution of all the freshwater Cottus of its spawned eggs are smallest among Japanese fresh- Japan. The present study was an effort to clarify the water Cottus (Kurawaka, 1976, 1992; Goto, 2001). It distribution of C. reinii in Lake Biwa throughout the ——————————————————————— year. *Corresponding author: [email protected]

− 13 − Distribution of Cottus reinii in Lake Biwa

Materials and Methods Chinai from February, 1997, to November, 1998, once per month (Fig. 1, Table 2). The nets were set In Lake Biwa, Cottus reinii is already known at 10-20 m depth perpendicular to the shore and the to inhabit deep offshore bottoms during winter captured fish were collected in the morning once (Mizutani et al., 1993). The first part of the present each day. One day’s take thus comprised the monthly study was therefore conducted from early summer to sample. autumn, in daytime. The fishing gear employed was To better comprehend the offshore distribution, a small-sized bottom-trawl net (height 1.4 m, width C. reinii were collected with a commercial bottom 1.3 m, depth 3.8 m with 2 mm mesh openings in the trawl-net (so-called “chyubiki ami”, mesh opening bottom net) with a pair of two-ropes 100 m or 300 m 2 mm) or cage-traps (so-called “ebi-tatsube”, mesh long (for details see Sakai et al., 2002). This net was opening of the bottom net 2 mm) from October, towed on the bottom at the several depths between 1996, to January, 1999, in one day per month except 2 and 40 m in shore and offshore of Hikone (Fig. 1, for July, August, September, and November, 1997, Table 1) for about 250 m during on the daytime of and May, and June, 1998. The chyubiki-ami was 12 June, 1 July, 1 August, and 24 and 25 October, used in the morning. 1996. At the same time, water temperature at several The fish were identified as C. reinii by their ex- depths was measured. ternal appearance and number of pectoral fin rays, In order to investigate the lake shore more fully, following Nakabo (1993). The specimens were fish were caught by a commercial set-net (so-called preserved in 10% formalin, and their standard “Eri”, mesh opening of the bottom net 4.3 mm ) length measured (except for some taken small-size at Imazu from March, 1996, to June, 1997, and at bottom-trawl net surveys). The fish collected by commercial set-net and trawl-net were sexed by ex- amination of gonads. The spawning season of C. reinii in Lake Biwa has been reported as March to April (Nakamura 1963) or from late February to early May (Goto 1995), so we defined “the spawning season” as February to April, “the post-spawning season” as May to July, “the non-spawning season” as August to October, and “the pre-spawning season” as November to January, and

Table 1. Seasonal differences in numbers of Cottus reinii caught by small trawl-net at different depths in Lake Biwa Depth (m) Date 2 5 10 20 30 40 12 June, 1996 0 0 1 94 25 - 1 July, 1996 0 0 2 600 197 394 Fig. 1. Map showing sampling sites. 1 and 2 are the set-nets 1 August, 1996 0 - 0 123 60 71* in Chinai and Imazu, respectively. 3-8 indicate the approximate area of commercial bottom trawlng (the 24 and 25 October, 1996 - - 0 0 14 24 numbers correspond to “Location No.” in Table 3). 9 is the * This sample was taken on 25 July, 1996. site of use of the small bottom trawl-net.

− 14 − Yasuhiro Fujioka, Akihisa Sakai and Atsuhiko Ide

Table 2. Seasonal differences in numbers and standard length of Cottus reinii caught by set-nets in Lake Biwa. Number of fish taken at Number of fish taken at Year Date 1 1 Size range (cm) set net 1* set net 2* 3 Mar. - 9 4.92-7.22 12 Apr. - 11 4.64-9.13 1996 3 May - 6 4.98-6.75 11 Jun. - 7 5.08-7.78 2 Jul. - 5 5.18-7.14 24 Feb. 25 3 3.61-8.96 (3.88-7.16)*3 4 Mar. 13 4 4.23-12.48 (5.22-11.85)*3 1 Apr. 14 24 3.84-8.87 (4.38-9.20)*3 1997 10 May (5 May)*2 20 3 4.63-9.05 (7.19-10.25)*3 16 Jun. - 11 5.91-9.52 27 Nov. 88 - 3.42-9.89 15 Dec. 66 - 3.06-10.92 7 Feb. 41 - 4.78-10.43 19 Mar. 43 - 4.69-9.72 27 Apr. 29 - 4.30-8.91 25 May 6 - 4.88-9.18 1998 24 Jun. 33 - 2.29-7.89 18 Jul. 20 - 3.05-8.53 2 Aug. 23 - 3.27-8.53 21 Nov. 53 - 3.36-9.47 *1 The locations of set-nets 1 and 2 are shown in Fig. 1. *2 The date in parentheses pertains to set-net 2. *3 The data in parentheses pertain to set-net 2. compared the sex ratios each season. Statistical anal- most fish (more than 91%) were smaller than 3 cm yses were conducted using the Chi-square test. SL at depth of 20-30 m in June-August surveys. The The samples used in the study have been deposit- mode of the body size distributions changed from ed at the Lake Biwa Museum (LBM), Kusatsu, Shi- 1-1.99 cm SL in June to 2-2.99 cm SL in July and ga, Japan (No.1210055406-1210055429). August, then to 3-3.99 cm SL in October at depths of 30 and 40 m. Water temperature distributions are Results shown in Fig. 3. Distinct thermoclines were detected at depths of less than 20 m in June-August, with the In shore and offshore surveys from early summer to water temperature colder than 12℃ at depths below autumn 20 m. The thermocline dropped to 18-26 m depth by Cottus reinii were caught deeper than 30 m from October, when water temperatures under 12℃ oc- June to October, not being taken at all at 5 m in June curred deeper than 24 m. and July, 2 and 10 m in August, and 10 and 20 m in October (Table 1). Fish were scarce at 10 m depth in Year-round in shore and offshore surveys by set-net June and July, while a large number of fish (>50) was and bottom trawl-net caught at 20 m in June-August and at 30 and 40 m in At the lake shore, C. reinii was collected by set- July-August. Body size was 1.01-10.23 cm SL and net in all months (except January, September, and

− 15 − Distribution of Cottus reinii in Lake Biwa

Fig. 2. Frequency distributions of standard length of Cottus reinii collected by small bottom trawl-net at depths of 20, 30, and 40 m in June, July, August, and October, 1996.

Table 3. Seasonal difference in numbers and standard length of Cottus reinii caught by bottom trawl-nets and cage-traps (so called "Ebi- tatsube") in Lake Biwa Location No. Number of Size range Year Date (see Fig. 1) Depth (m) trawl tows Number of fish (cm) 11 Oct. 8 40 1 141 3.26-10.23 1996 20 Nov. 6 70 8 52 3.48-8.61 16 Dec. 6 70 8 110 3.77-9.03 9 Jan. 6 70 8 51 4.01-9.92 10 Feb. 7 50 8 49 3.68-6.62 10 Mar. 5 50 8 54 4.22-6.99 20 Apr. 5 50 8 52 3.93-9.65 1997 11 May* 9 40 - 23 4.28-7.88 10 Jun.* 9 40 - 40 4.76-7.06 29 Oct. 7 30-80 3 46 3.03-10.87 6 Dec. 6 75 9 98 4.03-8.61 30 Jan. 6 73 9 60 3.70-9.25 23 Feb. 7 50 9 116 3.44-8.26 30 Mar. 5 58 2 134 3.51-8.84 22 Apr. 5 50 1 27 4.66-9.88 9 Jul. 8 20-40 3 18 2.14-5.66 1998 28 Aug.* 9 40 - 67 4.71-8.35 28 Sep.* 4 20 - 50 6.11-10.46 11 Oct. 4 40 8 51 5.70-9.20 25 Nov. 6 70 8 50 5.14-7.28 5 Dec. 3 80 8 51 4.93-7.53 1999 6 Jan. 6 70 8 78 3.65-11.09 * On these four dates, fish were caught by cage-traps (so called “Ebi-tatsube”).

− 16 − Yasuhiro Fujioka, Akihisa Sakai and Atsuhiko Ide

October; when commercial fishing is not done) for of water in early summer and tends to be distributed three years in succession, with body sizes of 2.29- deeper than 20 m thereafter. We may compare these 11.85 cm SL (Table 2). In the same way, C. reinii result with Lake Superior, one of the North Ameri- was caught by bottom trawl-net in all months for can Great Lakes, in which three species of sculpin, C. four years in succession on offshore bottom, with cognatus, C. ricei, and Myoxocephalus thompsoni, body sizes of 2.14-11.09 cm SL (Table 3). Among occur and are generally abundant at depths of greater the fish caught by set-net, significantly (p<0.05) fe- than 20 m (Dryer, 1966; Selgeby, 1988). Fujioka et male-biased sex ratios were observed in the spawn- al. (2014) reported that the occurrence of C. reinii ing season and the pre-spawning season in both is rare in the inflowing rivers of the South Basin of 1997 and 1998 (Table 4). Among those collected Lake Biwa, but relatively common in North Basin by bottom trawl-net, all the spawning seasons and streams, and attributed this to differences between pre-spawning seasons showed significantly p( <0.01) the North and South Basins in bathymetry and var- female-biased sex ratios, while the non-spawning season in 1996 and the post-spawning season in 1997 showed significant male bias, and the non-spawning season in 1998 showed significant female bias (Table 5).

Discussion

The present commercial trawl-net surveys re- vealed that C. reinii is abundant in the offshore bot- tom waters deeper than 40 m throughout the year in Lake Biwa. In addition, the results of the set-net and a small size bottom trawl-net surveys show that this species also dwells in coastal waters (10-20 m depth) at least from winter to summer (no data for Septem- Fig. 3. Seasonal changes in the water temperature profile of Lake ber). The fish is scarce at the coast in less than 10 m Biwa in 1996.

Table 4. Seasonal differences in sex ratios of Cottus reinii caught inshore by set-nets in Lake Biwa

Reproductive male/ 2 Year Duration season* ♂:♀ (male+female) χ March-April SS 8 : 12 0.40 0.8

February-April SS 19 : 64 0.23 24.4>p0.01

1997 May-June PoS 18 : 16 0.53 0.12

November-December PrS 64 : 90 0.42 4.39>p0.05

February-April SS 21 : 62 0.25 20.3>p0.01 May-July PoS 27 : 32 0.46 0.42

November PrS 19 : 34 0.36 4.25>p0.05 * SS, Spawning season; PoS, Post-spawning season; NS, Non-spawning season; PrS, Pre-spawning season.

− 17 − Distribution of Cottus reinii in Lake Biwa

Table 5. Seasonal differences in sex ratios of Cottus reinii caught offshore by bottom trawl-net in Lake Biwa

Reproductive male/ 2 Year Duration season* ♂:♀ (male+female) χ

1996 August-October NS 99 : 42 0.70 23.04

1996-1997 November-January PrS 30 : 183 0.14 109.9>p0.01

February-April SS 16 : 140 0.10 98.56>p0.01

1997 May-June PoS 40 : 23 0.63 4.59

October NS 25 : 21 0.54 0.35

1997-1998 December-January PrS 27 : 131 0.04 68.46>p0.01

February-April SS 46 : 231 0.17 123.56>p0.01

1998 July PoS 10 : 8 0.56 0.22

August-October NS 43 : 125 0.26 40.02>p0.01

1998-1999 November-January PrS 42 : 137 0.23 50.42>p0.01 * SS, Spawning season; PoS, Post spawning season; NS, Non spawning season; PrS, Pre-spawning season. ious physical phenomena. The South Basin is less as the adult habitat, the hatched larvae mast pass than 10 m, mostly less than 6 m deep, in contrast to through a period of planktonic existence after de- the 104 m deep North Basin. This difference affects scending rivers to the lake. Hitherto, there has been not only physical conditions but also biological rela- no data related to their duration and distribution in tionships. Although one of the factors related to fau- the plankton, and the timing and size of settlement nal distribution is water temperature, which becomes on the bottom. In the present study, juveniles caught lower with depth (Fig. 3), temperature is not likely by bottom trawl-net were larger than 1.01 cm SL, to be the main factor restricting the depth range of which suggests that C. reinii begin its benthic life C. reinii, because this fish inhabits a wide range of soon after reaching this size in June. Further, the temperatures (4.8-28.1℃) (Fujioka et al., 2014). numbers of juveniles captured was highest at 20 m in Nakamura (1975) and Goto (1989) mentioned that depth compared to others depth in June and August, C. reinii prey some small aquatic insects of bottom and this depth nearly corresponded with the bottom dwellers in Lake Biwa. Since Jesogamnmarus an- of the thermocline. Many fish juveniles such as “ayu” nandalei, which is an endemic amphipod, are abun- plecoglossus altivelis (Tanaka at al., 2002) and “isa- dant in offshore deep bottom of the lake (Ishikawa et za” Gymnogobius isaza (Sakai et al., 2002) gather al., 2004, Godo & Ban, 2007), the vertical distribu- at thermocline, where zooplankton is also abundant tion of C. reinii may be related to the food organism (Nagoshi, 1982). The habitat of juvenile may be re- for the fish. Further investigation is needed to clarify lated C. reinii to the distribution of zooplankton and the factor(s) affecting the depth distribution of C. the role of this fish in the food web. reinii in Lake Biwa. The depth at which C. reinii was predominantly The mode of fish size (SL) caught in coastal wa- caught sifted from 10 m in July to over 30 m in Oc- ters at 20 m depth in June was 1-1.99 cm. These tober. Such a depth change in habitat in juveniles juveniles are evidently underyearlings, because this has also been reported in C. extensus, a species en- month marks the end of the breeding season (Feb- demic to Bear Lake, Utah-Idaho, USA (Ruzycki et ruary to early May) of C. reinii (Nakamura, 1975; al., 1998), and G. isaza in Lake Biwa (Sakai et al., Goto, 1995). Since this species has as an amphi- 2001). Cottus reinii may expand its range into the dromous life cycle using the lake instead of the sea profundal zone around October after reaching a size

− 18 − Yasuhiro Fujioka, Akihisa Sakai and Atsuhiko Ide larger than 30 mm SL, coinciding to the body size of Association, in Chinai, Takashima, Shiga, to Mr. fish captured in commercial bottom-trawl nets (Table Yoshimitsu Kawata of Chomeiji, Omihachiman, Shi- 3). ga, and to Mr.Toshiya Ogama of Imazu, Takashima, In the present study, female-biased sex ratios Shiga, for providing the fish for this study. We thank were mostly observed during the pre-spawning and Dr. M. J. Grygier for his critical reading of the man- spawning seasons in fish collected at both inshore uscript, and staff of the Shiga Prefecture Fisheries and offshore sites. In the genus Cottus, mature Experiment Station for help. males stay in cavity under selected rocks during the breeding season and protect their fertilized eggs until References they hatch. Mature females, in contrast, prowl about seeking such spawning sites (Goto, 1994). This be- Berra, T. M., 2001. Order ; Sub- havioral difference between the sexes may explain order Cottidei. In Berra, T. M. (ed.), Freshwater this seasonal female bias in the catch. Fish Distribution: 366-370. Academic Press, San The bottom sediment in Lake Biwa is fine mud Diego. at depths beyond 20 m, while the shallow-water Dryer, W. R., 1966. Bathymetric distribution of fish substrate is predominantly sand on gradual slopes in the Apostle Islands Region, Lake Superior. T. and gravel, cobbles, and boulders (Kotani, 1971). American Fish. Soc., 95: 248-259. Thus C. reinii is reported generally to prefer to Fujioka, Y., Kido, Y. Uenishi, M. Yoshioka M. & gravel bottoms (Nakamura, 1975; Goto, 1989) and Kashiwagi M., 2014. Distribution of Cottus reinii in rivers this fish indeed dwells in riffles on gravel and Cottus pollux in rivers around Lake Biwa, bottoms, not in pools with sand and mud (Fujioka central Japan. Biogeography, 16: 31-37. et al., 2014). Judging from the present study, almost Fushimi, H., 1993. Influence of climatic warming C. reinii inhabit the mud by bottom of the lake, on the amount of snow cover and water quality of the same as C. extensus in Bear Lake in the U.S.A. Lake Biwa, Japan. Ann. Glaciol., 18: 257-260. (Ruzycki et al., 1998). These results suggest that Godo, M. & Ban, S., 2007. Effect of temperature on sediment type does not always limit the habitat and metabolic rates and horizontal distribution of an vertical distribution of fish. endemic amphipod Jesogammarus annandalei in The present study revealed that the offshore pro- Lake Biwa. Japn. J. Limnol., 68: 375-389 (in Jap- fundal zone of Lake Biwa is an important habitat for anese with English summary). C. reinii. This area is facing to a gradual decrease Goto, A., 1993. Reproductive styles and life-history in dissolved oxygen (Okamura, 2008), as a result of variations. In Goto , A., Tsukamoto, K. & Maeka- global warning (Fushimi, 1993). Thus C. reinii is wa, K.(ed.), Freshwater migrating between listed as an endangered fish at present (Ministry of rivers and sea: life-history and evolution: 141- the Environment of Japan, 2013). In order to protect 153. Tokai University Press, Tokyo. (in Japanese). it, it is important to preserve the offshore environ- Goto, A., 1995. Utsusemikazika Cottus reinii. In ments of this lake. Kawanabe, H., Mizuno, N., (eds) Freshwater fishes of Japan: 668 .Yamatokeikokusha, Tokyo. Acknowledgements (in Japanese). Goto, A., 2001. The mode of differentiation of mi- We are grateful to the Momose Fishery Cooperative gration patterns: sculpins. In Goto, A., & Iguch, K.

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