BioInvasions Records (2019) Volume 8, Issue 2: 369–378

CORRECTED PROOF

Research Article Seasonal occurrence of the alien freshwater sinensis (Sollaud, 1911) in lower reaches of a river in western Japan

Hidetoshi Saito1,*, Kimihiro Kometani2 and Atsuya Kodama1 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]

Citation: Saito H, Kometani K, Kodama A (2019) Seasonal occurrence of the alien Abstract freshwater shrimp Palaemon sinensis (Sollaud, 1911) in lower reaches of a river Palaemon sinensis, a shrimp native to China, has now been recorded in numerous in western Japan. BioInvasions Records freshwater zones in Japan. The present study is the first report of the seasonal 8(2): 369–378, https://doi.org/10.3391/bir. occurrence of P. sinensis in a river environment. Monthly field research was 2019.8.2.18 conducted from December 2015 to November 2016 at three sites in the lower reach Received: 18 September 2018 of the Seno River, Hiroshima Prefecture, western Japan. At Stn. 1, in a side pool of Accepted: 8 February 2019 the main river, P. sinensis was found throughout the year. Ovigerous females were Published: 29 April 2019 present there from April to July, and undifferentiated juveniles from July to September. At Stn. 2, at a side bank of the main stream, the was collected in Thematic editor: David Wong December, January, and August to November; water velocity when P. sinensis was Copyright: © Saito et al. collected ranged from 3 to 8.5 cm/s. At Stn. 3, in a tide pool in the estuary zone, the This is an open access article distributed under terms of the Creative Commons Attribution License shrimp was detected during months with relatively heavy precipitation (April and (Attribution 4.0 International - CC BY 4.0). June) and in September–November; the range of salinity when P. sinensis was found was 0.1–22.7 ppt. No ovigerous females or undifferentiated juveniles were OPEN ACCESS. collected in the main stream or in the estuary zone. Together, these findings suggest a pattern wherein P. sinensis eggs hatch in riverside pools from April to July, with individuals then growing to a sexually differentiated size before dispersing and entering the main river stream, from approximately August to November, after which time they are probably only passively transported with the current into the estuary zone.

Key words: distribution, estuary, landlocked shrimp, ovigerous females

Introduction Since the latter half of the 20th century, numerous species of caridean have been intentionally or unintentionally introduced from East Asia to different regions of the world, for instance via shipping (such as hull-fouling and ballast water), in water used for aquaculture, and through the ornamental fish trade. Species that have become exotics outside their range include Palaemon macrodactylus Rathbun, 1902, Macrobrachium nipponense (De Haan, 1849), M. dayanum (Henderson, 1893), P. modestus (Heller, 1862), and Neocaridina davidi (Bouvier, 1904) (Rodríguez and Suárez 2001; De Grave and Ghane 2006; Gorgin and Sudagar 2008; De Grave and Mann 2012; Ashelby et al. 2013; Klotz et al. 2013; Lejeusne et al. 2014 ).

Saito et al. (2019), BioInvasions Records 8(2): 369–378, https://doi.org/10.3391/bir.2019.8.2.18 369 Seasonal occurrence of alien freshwater shrimp Palaemon sinensis

The introduction to Japan of the freshwater palaemonid shrimp Palaemon sinensis (Sollaud, 1911) occurred when it was imported from China as live fishing bait, under the product name ‘Shirasa ebi,’ and was subsequently released by anglers (Niwa 2010; Saito et al. 2011, 2017; Saito 2017, 2018). Native to China, southeastern Siberia, and Sakhalin (Shen 1939; Shokita 1979; Liu et al. 1990; Kawai and Nakata 2011), P. sinensis was not reported in Japan before 1990 (Liu et al. 1990), but has since been detected in freshwater habitats in numerous prefectures (Oonuki et al. 2010, 2017; Imai and Oonuki 2014; Hasegawa et al. 2016; Saito et al. 2016; Suginami Ward 2016; Yoshigou and Yoshigou 2016; Imai and Oonuki 2017; Saito 2017, 2018; Saito et al. 2017; Shichiri et al. 2017; Chow et al. 2018; Hiraoka et al. 2018; Imai et al. 2018). Ecological information on P. sinensis in Japan includes observations of ovigerous females from May to September (Oonuki et al. 2010; Hasegawa et al. 2016; Saito 2018). P. sinensis has abbreviated larval development as an adaptation to freshwater life (Shen 1939). Therefore, it is difficult for the larvae to disperse towards the sea, unlike amphidromous river shrimps (Oonuki et al. 2010; Imai and Oonuki 2014). The lower reaches of rivers provide various habitats, such as the main stream and side pools, where the environment may be seasonally altered by rainfall. Previous studies in Japan conducted in spring reported that P. sinensis is restricted to lentic environments and does not appear in lotic and tidally influenced areas (Saito et al. 2016; Saito 2018). More recently, however, our preliminary research showed that P. sinensis appeared in the estuary zone of the Seno River, Hiroshima Prefecture, western Japan, in autumn. This raised queries about the temporal and spacial distribution of the shrimp in Japanese rivers. In the present study, monthly field research was conducted to confirm the seasonal occurrence of the alien shrimp P. sinensis at different sampling sites in the lower reach of the Seno River.

Materials and methods The Seno River is relatively short (length ~ 22.5 km) and flows into Hiroshima Bay, Hiroshima Prefecture, western Japan (Figure 1). Saito et al. (2016) conducted research at five sampling stations at different distances upstream from the river mouth (i.e. 19.5, 7.5, 4.8, 3.7 and 2.2 km), and P. sinensis was found in the lower reaches, at 4.8 and 3.7 km from the river mouth. In the present study, monthly field sampling, from December 2015 to November 2016, was conducted to collect shrimp at three different sites along the lower reach of the river (Figure 2). Stn. 1 was a lentic riverside pool, located 3 km upstream from the river mouth. Stn. 2 was a side bank of the main stream, near Stn. 1. There is a tide-stopping weir erected 2.2 km upstream from the river mouth; its height is 90 cm, and the water level breaches the weir at the mean high water of spring tides. Stn. 3, located 50 m

Saito et al. (2019), BioInvasions Records 8(2): 369–378, https://doi.org/10.3391/bir.2019.8.2.18 370 Seasonal occurrence of alien freshwater shrimp Palaemon sinensis

Figure 1. Location of the sampling sites on the Seno River, Hiroshima Prefecture, western Japan. Shaded areas on the map of Japan indicate prefectures where Palaemon sinensis has been found.

Figure 2. Photographs taken of the sampling locations on the Seno River, Japan. A: Stn. 1, B: Stn. 2, C: Tide-stopping weir, D: Stn. 3. Photo by H. Saito.

downstream from the weir, was a tide pool that appeared at low water in the estuary zone. Shrimp were collected while being visually searched out during the day using a D-shaped hand net (opening, 35 × 30 cm; mesh size, 2.5 mm; handle length, 165 cm), which was pulled around the submerged vegetation and near the river bottom, over an area of approximately 3 m2 at

Saito et al. (2019), BioInvasions Records 8(2): 369–378, https://doi.org/10.3391/bir.2019.8.2.18 371 Seasonal occurrence of alien freshwater shrimp Palaemon sinensis

Figure 3. Average monthly precipitation near the sampling sites (data provided by the Japan Meteorological Agency).

each site. Sampled shrimp were fixed in 10% formalin and stored in 70% alcohol, for later identification under a stereoscopic microscope (SMZ745T; Nikon, Tokyo, Japan), with reference to the descriptions of Imai and Oonuki (2014) and Toyota and Seki (2014). The carapace length of P. sinensis was measured from the orbital edge to the posterior margin of the carapace. Sex determination was made by noting the presence (males) or absence (females) of an appendix masculina on the second pleopod. Since that structure is not clearly visible in very small individuals (carapace length < 3.5 mm), they were categorized as undifferentiated juveniles. Females were further categorized in terms of their reproductive condition (ovigerous or non-ovigerous). Salinity and water temperature at the sites were measured with a handheld water-quality meter (YSI Model 85; YSI Inc., Ohio, USA). Water velocity at the surface was measured using the float method. Monthly precipitation over the study period ranged between 66.5 and 509.5 mm (Japan Meteorological Agency 2017), and rainfall was remarkably greater in April, June and September when compared with the past 30-year averages (Figure 3). A liner regression was applied to the relationship between water velocity and monthly precipitation, using Microsoft Excel 2010 software (Microsoft Japan Co., Ltd, Tokyo, Japan). Moreover, a multiple-comparison procedure with the Tukey-Kramer test was performed using Ekuseru-Toukei ver. 2015 software (Social Survey Research Information Co., Ltd, Tokyo, Japan) to evaluate statistical significance of the numbers of P. sinensis collected during three life-history terms, that is ‘before reproduction’ (December– March), ‘reproduction’ (April–July), and ‘after reproduction’ (August– November).

Results Environmental data for the sampling sites are shown in Supplementary material Table S1. Salinity was 0 ppt at both Stn. 1 and Stn. 2 over the course of the year; at Stn. 3, the salinity range was 0.1–22.7 ppt when P. sinensis

Saito et al. (2019), BioInvasions Records 8(2): 369–378, https://doi.org/10.3391/bir.2019.8.2.18 372 Seasonal occurrence of alien freshwater shrimp Palaemon sinensis

Figure 4. Relationship between monthly precipitation and water velocity at Stn. 2 (the side bank of the main stream).

were collected. At Stn. 2, water velocity ranged from 3 to 27 cm/s, with the highest values recoded in April and June; the range of water velocity when P. sinensis was found was 3–8.5 cm/s. Water velocity at that site showed a positive relationship with monthly precipitation (Figure 4). Supplementary material Table S2 lists the shrimp species collected at the different sampling sites; P. sinensis was collected at all three sites (349, 27, and 19 individuals at Stn. 1, Stn. 2, and Stn. 3, respectively). Neocaridina spp. were also dominant, and were collected at Stn. 1 (164 individuals) and Stn. 2 (1,085 individuals). Field observations were made of the microhabitats occupied by the dominant shrimps. Neocaridina spp. were mostly observed in submerged vegetation, whereas P. sinensis spent its time on sandy sediment as well as on submerged plants, but moved occasionally by swimming in the water column. The other shrimp species recorded during the study were P. paucidens De Haan, 1844 and Caridina leucosticta Stimpson, 1860, at both Stn. 1 and Stn. 3; and P. orientis Holthuis, 1950 and Macrobrachium nipponense, at Stn. 3 only (Table S2). Figure 5 shows the total number of P. sinensis collected at each site by life-history category. At Stn. 1, males (carapace length: 3.9–8.6 mm) and non-ovigerous females (3.5–10.7 mm) were collected in all months; ovigerous females (7.0–10.7 mm) were collected from April to July; and undifferentiated juveniles (2.0–3.4 mm) were collected in July to September. At Stn. 2, males (3.9–6.6 mm) and non-ovigerous females (5.2–7.8 mm) were collected in December, January, and August to November; no undifferentiated juveniles or ovigerous females were collected at this site on the side bank of the main stream. At Stn. 3, males (5.1–7.6 mm) and non- ovigerous females (4.5–10.0 mm) were collected in April, June, and September to November; no undifferentiated juveniles or ovigerous females were collected at this site in the estuary zone. Figure 6 depicts the numbers of P. sinensis collected in relation to their three life-history terms. At Stn. 1, the number of shrimp collected during the term ‘after reproduction’ (mean ± SD, 47.0 ± 8.5 individuals) was significantly larger than the numbers collected during the terms ‘before reproduction’

Saito et al. (2019), BioInvasions Records 8(2): 369–378, https://doi.org/10.3391/bir.2019.8.2.18 373 Seasonal occurrence of alien freshwater shrimp Palaemon sinensis

Figure 5. Numbers of Palaemon sinensis collected at the three sampling sites, categorized by life-history traits.

Figure 6. Comparison of the numbers of P. sinensis collected during different terms, namely: ‘before reproduction’ (December–March), ‘reproduction’ (April–July), and ‘after reproduction’ (August–November). Data are means ± standard deviations (n = 4). Asterisks show significant difference between two groups (Tukey-Kramer test: **p < 0.01, *p < 0.05).

(20.0 ± 17.1 individuals) and ‘reproduction’ (23.0 ± 9.1 individuals) (Tukey-Kramer test, p < 0.05). Likewise, at Stn. 2, the number of shrimp collected ‘after reproduction’ (5.8 ± 2.2 individuals) was significantly larger than the numbers collected ‘before reproduction’ (1.0 ± 1.4 individuals) and

Saito et al. (2019), BioInvasions Records 8(2): 369–378, https://doi.org/10.3391/bir.2019.8.2.18 374 Seasonal occurrence of alien freshwater shrimp Palaemon sinensis

‘reproduction’ (0 individuals) (Tukey-Kramer test, p < 0.01). In addition, at Stn. 3, the number of shrimp in the category ‘after reproduction’ (3.8 ± 2.9 individuals) significantly differed from the number in the category ‘before reproduction’ (0 individuals collected) (Tukey-Kramer test, p < 0.05).

Discussion Reports of the alien shrimp P. sinensis in Japan have increased since Imai and Oonuki (2014) were able to clarify the morphological differences between that species and the native shrimp P. paucidens. The shrimp has been variously collected in lentic environments, such as ponds, lakes, agricultural waterways, streams and riverside pools (Oonuki et al. 2010, 2017; Imai and Oonuki 2014, 2017; Hasegawa et al. 2016; Saito et al. 2016, 2017; Suginami Ward 2016; Yoshigou and Yoshigou 2016; Saito 2017, 2018; Shichiri et al. 2017; Chow et al. 2018; Hiraoka et al. 2018; Imai et al. 2018). Studies in springtime show that P. sinensis preferred narrow, low ranges of water velocity (0–2 cm/s) and salinity (0–0.1 ppt) (Saito et al. 2016; Saito 2018). In the present study, P. sinensis was found throughout the year in a lentic riverside pool. Additionally, the shrimp was collected at a side bank of the main river, where the stream velocity was 3–8.5 cm/s, in December, January, and August to November. Interestingly, it was also found in the estuary zone, in a tide pool with salinities of 0.1–22.7 ppt, in April, June and September to November. These findings suggest that the main habitat of P. sinensis in the Seno River is riverside pools, though it appeared occasionally in lotic and tidally influenced habitats. In China, spawning of P. sinensis was reported as occurring in May (Liu et al. 1990), and in the Russian Far East ovigerous females were observed during May and June (Kawai and Nakata 2011). In Japan, ovigerous females have been observed from May to September (Oonuki et al. 2010; Hasegawa et al. 2016; Saito 2018). Our findings thus agree with previous reports, as ovigerous females were observed from April to July. Undifferentiated juveniles, which seemed to be newly recruited individuals, were collected in the riverside pool from July to September. However, ovigerous females and undifferentiated juveniles were not found in the main stream or in the estuary zone. Hence, shrimp eggs obviously hatch out in riverside pools, and individuals seem to expand their local distribution by entering the main stream once they reach a sexually differentiated size. The present study also found a moderate number of P. orientis in the tidally influenced area; this species is typically distributed along coastlines, especially in estuarine waters (Chen and Hirano 1989). P. paucidens and C. leucosticta were collected in both the tidally influenced area and the freshwater riverside pool, while M. nipponense was collected only in the tide pool. These shrimps are considered amphidromous species which

Saito et al. (2019), BioInvasions Records 8(2): 369–378, https://doi.org/10.3391/bir.2019.8.2.18 375 Seasonal occurrence of alien freshwater shrimp Palaemon sinensis

migrate between rivers and the sea as they metamorphose (Shokita 1979; Armada et al. 1993; Nakata et al. 2010; Kawai and Nakata 2011; Saito et al. 2012; Toyota and Seki 2014; Chow et al. 2018). In contrast, P. sinensis and Neocaridina spp. are considered landlocked shrimps that are able to spend their entire life cycle in rivers (Shokita 1979; Oonuki et al. 2010; Saito et al. 2012; Toyota and Seki 2014). Although, Neocaridina spp. were collected only in freshwater areas, P. sinensis was additionally found in the tidally influenced area, in April, June and September–November. Previous studies established that Neocaridina shrimps may show positive stereotaxis to submerged vegetation, thereby improving their chance of remaining in freshwater in case of a flooding event (Niwa and Yokoyama 1993; Saito et al. 2012). However, our field observations revealed that P. sinensis spent their time on sandy sediments as well as on submerged plants, and moved occasionally by swimming in the water column. Since P. sinensis need not pass from freshwater to estuarine waters to complete its life history, the shrimp seems to have been passively transported into the estuary after heavy rainfalls, in April and June, when the water velocity attained 16.7– 27.0 cm/s. By expanding its distribution into the main stream during September–November, the shrimp increased its risk of being carried by the current beyond the tide-stopping weir and into the estuary. Interestingly, P. sinensis was found to survive even in a saline environment with 22.7 ppt. However, the shrimp would need to pass back over the weir to return to the upstream freshwater area and their prime habitat. Although the weir height was 90 cm, the water level exceeds this during spring tides. Climbing behavior that would be needed to surmount the weir has been observed in other caridean shrimps, such as C. leucosticta and Neocaridina denticulata (Niwa and Yokoyama 1997; Kawai and Nakata 2011). In view of these combined observations, P. sinensis in the Seno River are possibly able to return to the upstream freshwater zone with high tides. Niwa and Yokoyama (1997) suggested that the landlocked shrimp N. denticulata as well as amphidromous shrimps expand their distribution by migrating to upstream habitats. In the present study, P. sinensis inhabited the main stream approximately during the period of August– November, likely as part of a process that expanded its distribution to upstream areas. The shrimp has also been found in the Seno River upstream of Stn. 1 (Saito et al. 2016). Further field research might focus on the active movements of P. sinensis to upstream habitats.

Acknowledgements

We thank anonymous referees for careful reading our manuscript and for giving useful comments. This study was partly supported by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (KAKENHI) Grant Number 15K06932. We thank Edanz Group (www.edanzediting.com/ac) for editing a draft of this manuscript.

Saito et al. (2019), BioInvasions Records 8(2): 369–378, https://doi.org/10.3391/bir.2019.8.2.18 376 Seasonal occurrence of alien freshwater shrimp Palaemon sinensis

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Supplementary material The following supplementary material is available for this article: Table S1. Environmental data in the lower reach of Seno River. Table S2. Record of shrimp species collected in lower reach of Seno River. This material is available as part of online article from: http://www.reabic.net/journals/bir/2019/Supplements/BIR_2019_Saito_etal_SupplementaryMaterial.xlsx

Saito et al. (2019), BioInvasions Records 8(2): 369–378, https://doi.org/10.3391/bir.2019.8.2.18 378