BioInvasions Records (2016) Volume 5, Issue 2: 93–100 Open Access DOI: http://dx.doi.org/10.3391/bir.2016.5.2.06 © 2016 The Author(s). Journal compilation © 2016 REABIC

Research Article

Distribution of the invasive freshwater sinensis (Sollaud, 1911) in rivers of Hiroshima Prefecture, western Japan

1, 2 1 1 Hidetoshi Saito *, Aiko Yamasaki , Junpei Watanabe and Koichiro Kawai 1Graduate School of Biosphere Science, Hiroshima University, 1-4-4 Kagamiyama, Higashi-Hiroshima 739-8528, Japan 2Faculty of Applied Biological Science, Hiroshima University, 1-4-4 Kagamiyama, Higashi-Hiroshima 739-8528, Japan *Corresponding author E-mail: [email protected]

Received: 8 October 2015 / Accepted: 22 February 2016 / Published online: 21 March 2016

Handling editor: Vadim Panov

Abstract

The freshwater palaemonid shrimp, Palaemon sinensis was imported into Japan from China as live fishing bait, and its introduction has become a concern in Japanese freshwater areas. In the present study, field research was conducted to confirm the distribution of this invasive shrimp in eight rivers in Hiroshima Prefecture, western Japan. We found caridean shrimp, such as P. sinensis, Palaemon paucidens, Palaemon serrifer, Palaemon macrodactylus, Palaemon orientis, Macrobrachium nipponense, Caridina leucosticta, and Neocaridina spp.. P. sinensis was found in four rivers. A longitudinal distribution analysis showed that P. sinensis occurred in the lower reaches, whereas P. paucidens showed a wider distribution from the upper to the lower reaches. Palaemon sinensis occurred in a narrow range of stream velocity (0–2 cm/s) compared with that of P. paucidens (0–18 cm/s). P. sinensis density was negatively correlated with river velocity, indicating that this shrimp prefers a lentic water environment. Key words: fishing bait, introduction, lentic water, longitudinal distribution, palaemonid shrimp

Introduction mately 1,000 tons/year since 1969 (Hayashi 2001; Saito et al. 2011, 2014). Human-mediated introductions of aquatic organisms Freshwater palaemonid shrimp, Palaemon beyond their native range occurred with increasing paucidens De Haan, 1844 and Palaemon sinensis frequency during the latter half of the 20th century (Sollaud, 1911), formerly known as Palaemonetes (Carlton 1996; Rodríguez and Suárez 2001; sinensis (see Ashelby et al. 2012; De Grave and Iwasaki 2006; Ashelby et al. 2013). Although the Ashelby 2013), are supplied under the trade name shipping industry has received considerable attention “Shirasa ebi” in western Japan as live fishing as a dispersal mechanism for aquatic nuisance bait for rockfish, Sebastes inermis Cuvier, 1829, , many invasions have been linked to other sea bass, Lateolabrax japonicas (Cuvier, 1828), transfer mechanisms, such as the bait industry and black seabream, Acanthopagrus schlegelii (Weigle et al. 2005). Release of unused bait by (Bleeker, 1854) (Saito et al. 2011). “Shirasa ebi” anglers is an important vector for invasive is domestically collected in Japanese freshwater species (Haska et al. 2012; Kilian et al. 2012). areas, such as Lake Biwa, and is also imported Live fishing bait has been transported from from China at a rate of about 63 tons/year (Niwa Asian countries, mainly China, to European 2010). P. paucidens is a native species in Japan, countries, the United States, and Japan (Olive 1994; Korea, China, and Sakhalin (Hayashi 2000a), Gambi et al. 1994; Costa et al. 2006; Cohen 2012). whereas P. sinensis is distributed in China, More than 20 species of live fishing bait, such as Myanmar, southeastern Siberia, and Sakhalin (Liu polychaetes, bivalves, , and fish, have et al. 1990; Cai and Dai 1999; Cai and Ng 2002; been imported into Japan at a rate of approxi- Kawai and Nakata 2011). Since P. sinensis is

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Figure 1. Sampling locations in Hiroshima Prefecture, western Japan. For details see Supplementary material Table S1.

morphologically very similar to P. paucidens, the 10% formalin and identified with a stereoscopic shrimp trade inevitably uses both species as bait microscope (SMZ745T; Nikon, Tokyo, Japan). (Niwa 2010; Oonuki et al. 2010; Saito et al. 2011). We examined and identified both species based Although P. sinensis was not reported in Japan on the difference in carapace colour pattern (Imai before 1990 (Liu et al. 1990), this species was and Oonuki 2014). Other estuarine and freshwater discovered recently in freshwater ponds in central shrimp species were identified according to (Shizuoka Prefecture) and western (Kagawa Hayashi (1990, 1999, 2000a, b, c) and Toyota and Prefecture) Japan (Oonuki et al. 2010; Imai and Seki (2014). The atyid shrimp Neocaridina Oonuki 2014). Release of the bait by anglers is denticulate (De Haan, 1844) is distributed in thought to be why P. sinensis is found in freshwater western Japan (Hayashi 1990; Toyota and Seki areas. Therefore, P. sinensis may also be established 2014). However, non-native Neocaridina spp. are in other parts of Japan. However, introduction of imported as live fishing bait from China and shrimp remains poorly investigated in Japanese South Korea, and have been dispersed in various rivers. In the present study, field research was parts of Japan (Niwa 2010; Niwa et al. 2014). conducted to confirm the distribution of this species Because the of some Neocaridina spp. in rivers in Hiroshima Prefecture, western Japan is controversial (Shih and Cai 2007; Niwa et al. and to determine the relationships between 2010; Yoshigo 2011; Klotz et al. 2013), we distribution and environmental characteristics. denote Neocaridina shrimp as Neocaridina spp. Distance from the mouth of the river and Materials and methods altitude were calculated for each sampling point using Google Maps API v3. Salinity, dissolved We surveyed the Oze, Yahata, Ohota, Seno, Kurose, oxygen (DO), electrical conductivity, and water Kamo, Nuta, and Ashida Rivers in Hiroshima temperature were measured with a YSI model 85 Prefecture (Figure 1). Estuarine and freshwater water quality meter (YSI Inc., Ohio, USA). shrimp were sampled at five locations in each Velocity at the water surface was measured using river during March 2015. The shrimp was the float method. A stepwise multiple regression sampled using a D-shaped hand net (opening, 35 was performed using Ekuseru-Toukei ver. 2015 × 30 cm; mesh size, 2.5 mm; handle length, 165 cm). software (Social Survey Research Information Submerged vegetation and root masses in an Co., Ltd., Tokyo, Japan) to evaluate the effects approximate 1 m2 area at each station along the of the environmental variables (distance from the riverbanks were scooped with a net during the mouth of river, altitude, salinity, DO, electrical day. The shrimp was preserved immediately in conductivity and velocity) on P. sinensis density.

94 Distribution of invasive freshwater shrimp Palaemon sinensis

Figure 2. Occurrence of estuarine and freshwater caridean shrimp species in Hiroshima Prefecture.

Results was found were 0–1.5 for salinity, 6.48–9.27 mg/l for Do, 4.0–224.1 ms/m for electrical We collected caridean shrimp species, such as conductivity, and 0–18 cm/S for velocity. P. sinensis, P. paucidens, Palaemon serrifer (Stimpson, P. sinensis appeared mainly in lower reaches, 1860), Palaemon macrodactylus Rathbun, 1902, except the tidally influenced area (Figure 3). Palaemon orientis (Holthuis, 1950), Macrobrachium P. paucidens was widely distributed from the nipponense (De Haan, 1849). Caridina leucosticta upper to the lower reaches, including the tidally (Stimpson, 1860), and Neocaridina spp. in the eight influenced areas. The distributions of P. serrifer, rivers (Figure 2 and Supplementary material P. macrodactylus, P. orientis, and M. nipponense Table S1). P. sinensis was collected from the were restricted to the tidally influenced areas. Ohota (C4), Seno (D3 and D4), Kamo (F3 and C. leucosticta also occurred in tidally influenced F4), and Nuta Rivers (G4). Water quality data at areas and the adjacent freshwater area. Neocaridina the sampling sites where P. sinensis was found, spp. was widely distributed from the upper to the were 0 for salinity, 6.63–10.03 mg/l for DO, 6.0– lower reaches, except the tidally influenced area. 12.5 ms/m for electrical conductivity, and 0–2 The stepwise multiple regression between cm/S for velocity (Table 1). P. paucidens was found P. sinensis density and the environmental variables in all eight rivers (A1, A3, A4, B1, C4, D5, E1, (Fin = 2, Fout = 2) showed that of the predictor E2, F1, F5, G1, H1, H4, and H5). Water quality variables only velocity (F = 4.848, p = 0.041) data at the sampling sites where P. paucidens was selected as influential (Table 2).

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Figure 3. Longitudinal distributions of estuarine and freshwater caridean shrimp species The graph for each species was prepared based on shrimp collected from all rivers sampled.

Discussion River, it occurred in the mid-stream at 11 m of altitude and 17.0 km from the river mouth, ca. Although P. sinensis has been reported to inhabit 1.5 km upstream from the Takase dam that freshwater ponds in central and western parts of intercepts the flowing tide. Our results show that Japan (Oonuki et al. 2010; Imai and Oonuki 2014), P. sinensis has a narrow range of stream velocity occurrence of this species was also confirmed in (0–2 cm/s) compared with that of P. paucidens freshwater areas of four of the eight surveyed (0–18 cm/s). Stepwise multiple regression revealed rivers in western Japan; the Ohota, Seno, Kamo, that the density of P. sinensis was negatively and Nuta Rivers. In the last three rivers, it was correlated with water velocity. P. sinensis reportedly found in lower reaches at 3–9 m of altitude and occurs in lentic downstream environments of Far 2.0–4.8 km from the river mouth. In the Ohota East Russia (Kawai and Nakata 2011). In Japan,

96 Distribution of invasive freshwater shrimp Palaemon sinensis

Table 1. Physical environments at the sampling stations.

this introduced shrimp seems to be restricted to et al. 2012). In the present study, P. serrifer, P. lentic environments similar to the native habitats macrodactylus, and P. orientis occurred in the found in continental regions of China and Russia. tidally influenced areas. These species are marine The longitudinal distribution of shrimp in a river and estuarine shrimp with planktonic larval stages can be affected by river topography and species (Chen and Hirano 1989; Kim 2010; Lejeusne et al. life history (Shokita 1979; Suzuki et al. 1993; Saito 2014). The other caridean shrimp, such as

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Table 2. Resuts of stepwise multiple regressions of P. sinensis density with environmental variables.

C. leucosticta, M. nipponense, P. paucidens, From the latter half of the 20th century, caridean Neocaridina spp., and P. sinensis had different shrimp species, such as P. macrodactylus, M. nippo- distributional patterns. Caridean shrimp species nense, Macrobrachium dayanum (Henderson, 1893), that inhabit lotic environments are classified into Palaemon modestus (Heller, 1862) and two types based on their methods of adaptation, Neocaridina davidi (Bouvier, 1904) have been i.e., amphidromous shrimp species that metamorphose reported to be introduced intentionally or in a marine environment and lay smaller eggs, unintentionally from East Asian countries worldwide and landlocked shrimp that lead their entire life (Rodríguez and Suárez 2001; De Grave and history in a river and lay fewer large eggs Ghane 2006; Gorgin and Sudagar 2008; De Grave (Shokita 1979). C. leucosticta and M. nipponense and Mann 2012; Ashelby et al. 2013; Klotz et al. were collected in the tidally influenced areas 2013; Lejeusne et al. 2014). In Japan, several and/or adjacent freshwater area. These shrimp are non-native Neocaridina spp. have been imported considered to be diadromous and migrate between from China and South Korea for use as live the river and sea to spawn (Armada et al. 1993; fishing bait together with the ectosymbiont Kawai and Nakata 2011; Saito et al. 2012; Toyota annelid, Holtodrilus truncatus (Liang, 1963), and and Seki 2014). In fresh water areas, landlocked later dispersed and settled after being discarded shrimp, such as P. sinensis, P. paucidens and into Japanese freshwater environments by anglers Neocaridina spp. were distributed and lay fewer (Niwa 2010; Niwa et al. 2014). P. paucidens and large eggs (Shokita 1979; Shih and Cai 2007; P. sinensis are supplied under the trade name Oonuki et al. 2010; Toyota and Seki 2014). These “Shirasa ebi” in western Japan as live fishing bait shrimp are important components of aquatic (Niwa 2010). P. paucidens has been evaluated as a ecosystems, playing a key role at intermediate target aquaculture species in various parts of tropic levels, as consumers of algae, detritus and Japan for food and fishing bait (Ogawa and small insects, and as prey of many fishes (Kawai Kakuda 1988). Since traders and fishermen are and Nakata 2011; Puspitasari 2013). In the six unaware of the difference between P. paucidens sampling stations where P. sinensis was found, and P. sinensis (Saito et al. 2011; Imai and Oonuki Neocaridina spp co-occurred at all stations, but 2014), P. sinensis will be mixed in shrimp seed P. paucidens appeared only one station. Although for P. paucidens aquaculture. Therefore, it is P. paucidens can live in lentic downstream environ- possible that P. sinensis will become established ments, there is a possibility that its distribution via not only release by anglers but also escape was narrowed by P. sinensis. Further researches from shrimp farms, so further investigations are are needed to clarify the invasion effects of P. necessary to confirm the occurrence of this species, sinensis on the native shrimp (e.g., competition particularly in areas where “Shirasa ebi” has been with them or ecosystem change via the food chain). cultured.

98 Distribution of invasive freshwater shrimp Palaemon sinensis

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Supplementary material The following supplementary material is available for this article: Table S1. Records of Palaemon sinensis and other caridean shrimp species, collected in Hiroshima Prefecture, western Japan.

This material is available as part of online article from: http://www.reabic.net/journals/bir/2016/Supplements/BIR_2016_Saito_etal_Supplement.xls

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