Fish Sci (2014) 80:1231–1239 DOI 10.1007/s12562-014-0797-8
ORIGINAL ARTICLE
Biology
Utilization patterns of estuarine and marine habitats by the halfbeak Zenarchopterus dunckeri at Iriomote Island, southern Japan, evaluated from otolith microchemistry Takahiro Kanai • Kusuto Nanjo • Kodai Yamane Yosuke Amano • Hiroyoshi Kohno • Yoshiro Watanabe • Mitsuhiko Sano
•
Received: 23 June 2014 / Accepted: 2 August 2014 / Published online: 11 September 2014 Ó Japanese Society of Fisheries Science 2014
Abstract Estuarine and marine habitat use patterns in the halfbeak Zenarchopterus dunckeri were examined at Iriomote Island, southern Japan, by analyzing otolith Li/Ca and Sr/Ca ratios. The ranges of both Li/Ca and Sr/Ca ratios in juvenile Z. dunckeri from the maximum (30 psu) to minimum (0.5 psu) salinity levels of brackish water estimated from rearing experiments, were compared with those of wild individuals collected from upstream and downstream stations in the Urauchi River estuary. The majority of wildcaught individuals had invariable Li/Ca and Sr/Ca ratios along an otolith transect from the core to the posterior edge, which fell within the otolith Li/Ca and Sr/Ca ranges estimated for estuarine individuals in the rearing experiments, suggesting that such individuals developed within the estuary without migrating to a marine environment at any time, although some downstream-dwelling fish had higher otolith elemental ratios than the predetermined estuarine ranges in the mid transect section. The latter fish may have been accidentally flushed from the estuary into the sea by heavy flood events, subsequently returning to the estuary. The overall results suggested that Z. dunckeri is essentially an estuarine resident, completing its life cycle within an estuarine system. T. Kanai (&) M. Sano Department of Ecosystem Studies, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi, Bunkyo, Tokyo 113-8657, Japan e-mail:
[email protected] K. Nanjo K. Yamane Y. Amano Y. Watanabe Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba 277-8564, Japan H. Kohno Okinawa Regional Research Center, Tokai University, Uehara, Taketomi, Okinawa 907-1541, Japan
Keywords Estuary Habitat use pattern Laser ablation inductively coupled plasma mass spectrometry (LA-ICPMS) Lithium/calcium ratio Movement Otolith microchemistry Strontium/calcium ratio Zenarchopterus dunckeri
Introduction Tropical and subtropical estuaries often support many fish species, including a number of commercial importance (e.g., [1–3] ). Based on estuarine use patterns throughout their life histories, fishes occurring in estuaries can be classified into several categories, including marine migrant species that spawn at sea and enter estuaries as juveniles (often in large numbers), and estuarine species that complete their entire life cycle within the estuarine environment (estuarine residents) or have larval stages completed outside the estuary before returning to estuaries for growth and reproduction (estuarine migrants) [4]. Since marine migrants are often dominant in fish assemblages in tropical estuaries [5], previous studies have emphasized their estuarine use patterns and/or movements between marine and estuarine environments, thereby suggesting the importance of tropical estuaries as nursery areas for many marine fishes (e.g., [6–9]). In contrast to marine migrant species, however, the degree of residency and habitat use patterns for estuarine species (i.e., whether an estuarine resident or migrant between estuarine and marine habitats) have been little examined [10]. The halfbeak Zenarchopterus dunckeri is widely distributed in tropical estuaries in the Indo-West Pacific region, growing to about 130 mm standard length (SL) [11], although it has been listed as a near threatened species on the Red List of the Ministry of the Environment, Japan
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(http://www.env.go.jp/press/file_view.php?serial=21437& hou_id=16264; accessed 28 July 2014). This species has been considered as an estuarine resident due to several growth stages from juveniles to adults having been observed within estuaries [12–14]. Such observational information, however, is circumstantial, the estuarine residential status of Z. dunckeri remaining uncertain. Because fish otoliths incorporate various elements chronologically from ambient water, permanently recording environmental variations experienced over the individual’s entire lifespan [15], the elemental composition of otoliths reflects various environmental factors, such as salinity and the elemental composition in ambient water at the time of deposition (e.g., [16–18]). Accordingly, microchemical analysis of otoliths provides a powerful tool for elucidating migration and habitat use patterns of fishes which utilize both freshwater and marine environments [15]. In particular, strontium/calcium ratios of otoliths have been commonly used for examining habitat use patterns (i.e., migration) of many diadromous fishes [19, 20], such as European eel [21], Japanese eel [22] and American shad [23, 24]. However, few studies of habitat use patterns of estuarine fishes have been reported, due to the difficulty in reconstructing periods of estuarine and marine occupation from otolith Sr/Ca ratios, ambient Sr/Ca composition often being similar between estuarine and marine environments [25]. Recently, however, Hicks et al. [26] found otolith Li/Ca ratios of laboratoryreared amphidromous galaxiid fishes to be positively related to a more precise salinity gradient, suggesting such ratios to be potentially useful for exploring estuarine use by fishes [26, 27]. However, the absorption rate of ambient elements into otoliths is species-specific [28]. Accordingly, validation experiments examining the responses of otolith element/Ca ratios in targeted species under controlled rearing conditions are needed in order to precisely interpret the otolith elemental signatures of their wild counterparts. The objective of the present study was to clarify habitat use patterns in Z. dunckeri at Iriomote Island, southern Japan, using both otolith Li/Ca and Sr/Ca ratios. A laboratory rearing experiment was conducted using juvenile Z. dunckeri, to determine the values and ranges of such ratios responding to predetermined ambient salinity levels (brackish and sea water). These ratios were then compared with those of wild-caught individuals to determine whether or not the species moved between estuarine and marine areas.
Materials and methods Study site The study was conducted in the Urauchi River (24°240 N, 123°460 E), situated on the northern side of Iriomote Island,
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Urauchi Bay
Urauchi River 24 20’ N
Iriomote Island
123 50’E
ORRC
Bay
Urauchi River
Downstream
Midstream
Upstream
1km
Fig. 1 Map of the Urauchi River estuary, Iriomote Island, Ryukyu Islands, Japan. Open squares fish sampling station (downstream and upstream); closed circles water measuring station (bay, downstream, midstream and upstream); closed square Okinawa Regional Research Center, Tokai University (ORRC)
Ryukyu Islands, Japan (Fig. 1). With a drainage area of 54 km2, the river is 39 km in length (the longest river in Okinawa Prefecture), feeding into Urauchi Bay. The brackish water zone ranges 8 km upstream from the river mouth, with mangrove forests dominated by the red mangrove Rhizophora stylosa. Tidal range within the river is approximately 1.5 m, prop roots being inundated at high tide and partially exposed at low tide. Fish sampling stations were established in the lower and upper regions (2 and 10 km from the river mouth, respectively) of the river (hereafter referred to as downstream and upstream stations, respectively) (Fig. 1). In addition, to determine appropriate salinity treatment levels in the rearing experiment, salinity and water temperature were measured at four stations across a salinity gradient (marine bay, downstream, midstream and upstream, Fig. 1, n = 3 per station) by Hydrolab Quanta Multiparameter Sonde (Hydrolab, Denver, CO, USA), during ebb tide in June 2013 (Table 1).
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Table 1 Mean (± SD, n = 3) salinity and water temperature at each station in the Urauchi River in June 2013
Sample collection and preparation
Station
To determine habitat use patterns of Z. dunckeri over the entire life history of the species, wild individuals were collected from the downstream and upstream stations in the study river. Twenty-five individuals (79.2 ± 23.1 mm SL) were captured at the downstream station using a dip net and cast net in August 2013. Additionally, six individuals (75.3 ± 3.5 mm SL) were collected from the upstream station in October 2013. The SL of each fish was measured and the whole specimen frozen for subsequent otolith analysis.
Salinity (psu)
Upstream
7.0 ± 0.8
Water temperature (°C) 24.5 ± 0.2
Midstream
15.1 ± 0.4
26.7 ± 0.8
Downstream
25.1 ± 0.6
28.7 ± 1.6
Bay
32.2 ± 0.3
27.3 ± 0.6
Rearing experiment A laboratory rearing experiment was conducted between June and July 2013 in order to determine the values and ranges of otolith Li/Ca and Sr/Ca ratios in Z. dunckeri across a salinity gradient. Prior to the experiment, 40 juveniles of the species were collected from the downstream station using a dip net and their SLs measured (mean ± SD 7.3 ± 0.8 mm SL). Alizarin complexone (ALC) was dissolved at a concentration of 50 mg/l in four small tanks (20 l volume) with salinity adjusted to 7, 15, 25 and 32 psu, respectively, corresponding to the levels determined at each of the four stations in the study site (Table 1). All juveniles collected were randomly allocated to the tanks (10 individuals per tank) and exposed to ALC solution for 24 h under aeration, thereby marking the otoliths. Subsequently, all fish in each tank were transferred to a larger tank (60 9 30 9 36 cm, 65 l volume) with the same salinity level as before (i.e., 7, 15, 25 and 32 psu, respectively), adjusted by combining natural seawater with tap water that had been aged for several days to allow chlorine to dissipate. Fish were maintained for 30 days, being fed twice daily with commercial pellets (Otohime B2, Marubeni Nisshin Feed, Tokyo, Japan). Salinity was checked every day and controlled by adding seawater or aged tap water. A constant water temperature (ca. 28.0 °C) and photoperiod (13L/11D) were maintained across all tanks during the experiment. Rearing water was exchanged with natural seawater and aged tap water, approximately 30 % of the tank volume being replaced every 5 days. After the experiment, the SL of each individual was measured and the specimen frozen until otolith chemical analyses. All of the fish grew during the experiment (35.2 ± 4.1 mm SL), with 100 % survival. To assess whether otolith microchemistry was influenced more by ambient element/Ca or absolute ambient element concentrations, rearing water was sampled from each tank on the first (1), middle (15) and last (30) days of the experiment (i.e., n = 3 for each tank). The water was filtered through 1.2-lm glass fiber filters (Whatman GF/C, GE imagination at work), stored in acid-washed polypropylene bottles, and acidified (1 %) using concentrated ultrapure HCl (Wako Pure Chemical Industries, Osaka, Japan).
Otolith preparation and analysis Both left and right sagittal otoliths were extracted from all reared and wild-caught individuals. The otoliths were cleaned with Milli-Q water for 5 min in an ultrasonic bath, rinsed several times in Milli-Q water, and then air-dried and placed in a clean plastic case. Prior to the elemental analysis, the left otolith was embedded in enamel resin, mounted on a glass slide and ground to the core using sandpaper (800 lm) and lapping films (12, 3 and 0.5 lm) (3 M, Saint Paul, MN, USA). Finally, it was cleaned for 10 min in an ultrasonic bath, rinsed several times in Milli-Q water and then air-dried. The elemental composition of 10 otoliths per salinity treatment (tank) in the rearing experiment (total 40 otoliths) was analyzed. Three elements (Li, Ca and Sr) were measured for each otolith by laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS), which coupled a NWR-193 excimer laser ablation system (New Wave Research, Fremont, CA, USA) to ICP-MS (7700CS, Agilent, Tokyo, Japan). Each otolith of the reared individuals was ablated by a scanning spot laser beam (diameter 30 lm) at the posterior edge region outside the ALC ring (250–300 lm distant from the otolith core), and the elemental data for each otolith presented as the average of three scanning spots. Each otolith of the wild-caught individuals (n = 31) was also ablated by a scanning spot laser beam (diameter 30 lm) at 40-lm intervals along the transect from the otolith core to the posterior edge, the number of laser spots varying with the radius of each otolith (18–44 spots). Elemental composition was determined according to Yamane et al. [29, 30]. The frequency of the laser beam, and laser energy were 10 Hz and 7.05 J/ cm2, respectively. Background levels and standards were examined before and after each scan. Ca was used as an internal standard, all elemental data being expressed in terms of their molar ratio relative to calcium. The detection limits (in mmol/mol) achieved in this study, which were calculated on the basis of 3 SD from the mean blank count, were 0.0021 for Li/Ca and 0.000062 for Sr/Ca. Li and Sr contents were above the detection limits for all samples. Calibration from the signal intensity to the element was
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Table 2 Mean (± SD, n = 3) water elemental concentration (Li, Ca and Sr), Li/Ca and Sr/Ca in each salinity treatment in the rearing experiment
0.014
Treatment (psu)
Salinity
Concentration
(psu)
Li (ng/g)
Li/Ca (mmol/mol)
Sr/Ca (mmol/mol)
7.2 ± 1.0
11.8 ± 0.3
61.1 ± 0.6
909.3 ± 12.7
1.12 ± 0.02
6.81 ± 0.03
52.3 ± 0.5
168.1 ± 1.4
2,632.6 ± 13.2
1.80 ± 0.01
7.16 ± 0.02
25
25.1 ± 1.0
83.5 ± 2.7
267.9 ± 5.9
4,486.5 ± 65.1
1.80 ± 0.02
7.66 ± 0.06
32
32.2 ± 1.0
142.2 ± 7.7
398.3 ± 14.6
6,432.7 ± 134.6
2.06 ± 0.04
7.39 ± 0.13
0.008 0.006 0.004 0.002 0
Sr/Ca (mmol/mol)
Li/Ca (mmol/mol)
14.9 ± 1.0
0.010
10
Sr (ng/g)
7
0.012
0
Ca (lg/g)
15
(a)
8
Ca ratio
20
30
40
(b)
et al. [30]. Calibration from the signal intensity to the element was performed using 4 liquid standards: JSAC 0301-3 and JSAC 0302-3, distributed by the Japan Society for Analytical Chemistry (Tokyo, Japan), ICP Multi Element Standard Solution X, distributed by Merck Millipore (Darmstadt, Germany) and coastal seawater from Miyako Bay, Iwate Prefecture, Japan, with known elemental concentrations (Yamane et al., unpublished data). Liquid standards and instrument blanks of 1 % HNO3 were analyzed for every 8 samples. Beryllium, scandium, indium and bismuth were added to all samples and standard solutions (to 4.5 lg/l) as an internal standard to correct for instrumental drift. An internal laboratory seawater standard was used to assess measurement reproducibility. Mean estimates of reproducibility (%, relative standard deviation) were 1.65 for Li/Ca and 2.72 for Sr/Ca.
6
Statistical analysis
4 0
10
20
30
40
Salinity
Fig. 2 Mean otolith a Li/Ca and b Sr/Ca ratios in Zenarchopterus dunckeri for each of four salinity treatments in the rearing experiment (n = 10/treatment). Error bars indicate SD. Statistical differences indicated by a, b, c and d (post hoc Tukey–Kramer test, p \ 0.05)
performed using 3 standard materials: NIST SRM 612 standard glass, distributed by the National Institute of Standards and Technology (Gaithersburg, MD, USA), and pressed pellets of certified reference materials [powdered coral (JCp-1) and powdered giant clam (JCt-1)], distributed by the National Institute of Advanced Industrial Science and Technology (Tsukuba, Japan) [31]. Mean estimates of precision (%, relative standard deviation) based on the JCp1 standard were 1.86 for Li/Ca and 2.22 for Sr/Ca.
Before statistical analysis, all elemental data were examined for normality and homogeneity of variance using either Bartlett’s normality test (a = 0.05) or the Kolmogorov–Smirnov test (a = 0.05). Since normality and homogeneous variance were confirmed for all data after transformation [log(x ? 1)], parametric one-way analyses of variance (ANOVAs) were used to examine differences in elemental concentration and composition of rearing water, and elemental composition of the otoliths of reared individuals among the salinity treatments (tanks). When significant differences were recognized (p \ 0.05), post hoc Tukey–Kramer tests were applied. In order to estimate the values and ranges of otolith Li/ Ca and Sr/Ca ratios responding to the whole brackish water salinity range (0.5–30 psu) [32], linear regressions were performed, using otolith element/Ca of the reared individuals from each salinity treatment.
Water analysis Results The elemental composition of rearing water samples (Li, Ca and Sr) was measured by solution-based ICP-MS. These elements were chosen on the basis of their detection limits (in mg l-1): 0.000021 for Li, 0.092 for Ca and 0.00024 for Sr. All analytical procedures were performed according to Yamane
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Elemental composition of rearing water Absolute concentrations of Li and Sr in the rearing water increased significantly with increasing salinity (one-way
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ANOVA, F = 3490, p \ 0.001 for Li; F = 6685, p \ 0.001 for Sr), Tukey–Kramer tests detecting significant differences among all treatment pairs for each element (p \ 0.05) (Table 2). Li/Ca was highest in 32 psu and lowest in 7 psu (one-way ANOVA, F = 576.2, p \ 0.001; Tukey–Kramer test, p \ 0.05), although no significant difference was detected between 15 and 25 psu (p = 0.999). Sr/Ca was highest in 25 psu and lowest in 7 psu (one-way ANOVA, F = 156.3, p \ 0.001; Tukey– Kramer test, p \ 0.05 for all pairs) (Table 2). Elemental composition of reared fish otoliths Otolith Li/Ca ratios of the reared individuals increased with salinity, being highest in 32 psu and lowest in 7 psu (one-way ANOVA, F = 219.5, p \ 0.001; Tukey–Kramer test, p \ 0.05 for all pairs) (Fig. 2a). A similar tendency was found for Sr/Ca (one-way ANOVA, F = 21.8, p \ 0.001), but with no significant difference between 15 and 25 psu (Tukey– Kramer test, p = 0.816; p \ 0.05 for other pairs) (Fig. 2b).
Elemental composition of wild-caught fish otoliths Chronological profiles of Li/Ca and Sr/Ca ratios along otolith transects revealed different trends between fish collected from the upstream and downstream stations. Average Li/Ca and Sr/Ca values of the upstream fish
(a) Li/Ca (mmol/mol)
0.025 0.020 0.015 0.010 0.005 0
SW BW
Sr/Ca (mmol/mol)
12
SW
9
6
BW FW
3 0
500
1000
1500
Distance from otolith core (µm)
(b) 0.0250
Male, 79.9 mm SL
Male, 76.7 mm SL
Male, 77.2 mm SL Li/Ca
Li/Ca
Li/Ca
Sr/Ca
Sr/Ca
Sr/Ca
0.0125 0
Element/Ca (mmol/mol)
Fig. 3 Li/Ca and Sr/Ca profiles along a transect from the core to the posterior edge of the otolith in wild Zenarchopterus dunckeri collected from the upstream station. a Mean of all fish collected (n = 6); error bars indicate SD. b Each individual fish (four males and two females). Gray areas indicate range of each otolith elemental ratio estimated for estuarine individuals from the linear regression equations in the rearing experiment. SW seawater, BW brackish water, FW freshwater
Significant linear regressions were found between otolith elemental ratios and salinity (SAL): Li/ Ca = 0.00036SAL - 0.00029 (r2 = 0.882, p \ 0.001, n = 40, Fig. 2a) and Sr/Ca = 0.075SAL ? 4.22 2 (r = 0.627, p \ 0.001, n = 40, Fig. 2b). From these equations, otolith Li/Ca ratios at 0.5 and 30 psu were estimated to be 0 and 0.011 mmol/mol, respectively, and otolith Sr/Ca ratios 4.26 and 6.47 mmol/mol, respectively. In the following otolith transect analyses, therefore, such estimated ranges of Li/Ca (0–0.011 mmol/mol) and Sr/Ca (4.26–6.47 mmol/mol) were used to assess whether or not the wild-caught fish had remained in the estuarine environment throughout their life histories.
12 9 6 3 0 0.0250
500
1000
1500
Male, 74.6 mm SL
0
500
1000
1500
0
500
1000
1500
Female, 69.6 mm SL
Female, 73.8 mm SL Li/Ca
Li/Ca
Li/Ca
Sr/Ca
Sr/Ca
Sr/Ca
0.0125 0 12 9 6 3 0
500
1000
1500
0
500
1000
1500
0
500
1000
1500
Distance from otolith core (µm)
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(n = 6) varied little from the core to the posterior edge of the otoliths, keeping mostly within the ranges of otolith Li/ Ca (0–0.011 mmol/mol) and Sr/Ca (4.26–6.47 mmol/mol) estimated for estuarine individuals in the above regression analysis (hereafter, estuarine range) (Fig. 3). For the downstream fish (n = 25), which had higher otolith Li/Ca ratios compared with those of upstream fish (Figs. 3, 4, 5), along-transect profiles of Li/Ca and Sr/Ca were classified into two types (hereafter, type 1 and type 2), based on the intensity (i.e., frequency and period) of marine habitat use. Mean otolith Li/Ca and Sr/Ca ratios of type 1 fish (72 % of downstream fish) were relatively constant, remaining mostly within estuarine ranges along the entire otolith transect (Fig. 4a), although some individuals (28 % of type 1 fish) had temporally spiked values beyond estuarine ranges in the middle section of the transect (e.g., female with 97.1 mm SL in Fig. 4b). Of type 2 fish (28 % of downstream fish), on the other hand, average otolith Li/Ca and Sr/Ca ratios in the middle transect section were successively higher than the estuarine ranges, indicating continuous marine habitat use, although the values
Discussion The rearing experiment in the present study demonstrated that both otolith Li/Ca and Sr/Ca ratios in reared Z. dunckeri responded positively to the salinity gradient, being consistent with previous studies (e.g., [24, 33] ), although otolith Sr/Ca values did not differ significantly between 15 and 25 psu. This result is considered reliable, due to other potentially confounding factors, such as rearing temperature, fish diets and analyzed regions of otoliths (posterior edge region of 250–300 lm distant from the core), being well controlled in the experimental context, so as to minimize their effects on otolith elemental composition [34–36]. Otolith Li/Ca and Sr/Ca ratios of reared Z. dunckeri differed between the estuarine (7, 15 and 25 psu) and marine (32 psu) environments, with responses to the finer
Li/Ca (mmol/mol)
(a) 0.025 0.020 0.015 0.010 0.005 0
SW BW
12
Sr/Ca (mmol/mol)
Fig. 4 Li/Ca and Sr/Ca profiles along a transect from the core to the posterior edge of the otolith in wild Zenarchopterus dunckeri collected from the downstream station (type 1). a Mean of all fish collected (n = 18); error bars indicate SD. b Individual results from 6 fish (three males and three females), selected arbitrarily from a. Gray areas indicate range of each otolith elemental ratio estimated for estuarine individuals from the linear regression equations in the rearing experiment. SW seawater, BW brackish water, FW freshwater
of the otolith core and edge regions were mostly within estuarine ranges (Fig. 5).
SW
9 6
BW
3
FW 0
450
900
1350
1800
Distance from otolith core (µm)
(b) 0.0250
Male, 103.8 mm SL
Male, 92.8 mm SL
Male, 101.5 mm SL
Li/Ca
Li/Ca
Li/Ca
Sr/Ca
Sr/Ca
Sr/Ca
Element/Ca (mmol/mol)
0.0125 0 12 9 6 3 0 0.0250
900
1800
0
900
1800
Female, 97.1 mm SL
Female, 98.1 mm SL
0
900
1800
Female, 95.5 mm SL
Li/Ca
Li/Ca
Li/Ca
Sr/Ca
Sr/Ca
Sr/Ca
0.0125 0 12 9 6 3 0
900
1800
0
900
1800
Distance from otolith core (µm)
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0
900
1800
Fish Sci (2014) 80:1231–1239
Li/Ca (mmol/mol)
(a) 0.025 0.020 0.015 0.010 0.005 0
SW BW
12
Sr/Ca (mmol/mol)
Fig. 5 Li/Ca and Sr/Ca profiles along a transect from the core to the posterior edge of the otolith in wild Zenarchopterus dunckeri collected from the downstream station (type 2). a Mean of all fish collected (n = 7); error bars indicate SD. b Individual results from 6 fish (three males and three females), selected arbitrarily from a. Gray areas indicate range of each otolith elemental ratio estimated for estuarine individuals from the linear regression equations in the rearing experiment. SW seawater, BW brackish water, FW freshwater
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9
SW
6
BW FW
3 0
450
900
1350
1800
Distance from otolith core (µm)
(b) 0.0250
Male, 97.5 mm SL
Male, 100.6 mm SL
Male, 85.8 mm SL
Li/Ca
Li/Ca
Li/Ca
Sr/Ca
Sr/Ca
Sr/Ca
Element/Ca (mmol/mol)
0.0125 0 12 9 6 3 0 0.0250
900
1800
Female, 94.3 mm SL
0
900
1800
0
900
1800
Female, 79.1 mm SL
Female, 90.9 mm SL
Li/Ca
Li/Ca
Li/Ca
Sr/Ca
Sr/Ca
Sr/Ca
0.0125 0 12 9 6 3 0
900
1800
0
900
1800
0
900
1800
Distance from otolith core (µm)
estuary salinity gradient (i.e., 7, 15 and 25 psu) being apparent for Li/Ca (Fig. 2). An approach using both otolith Li/Ca and Sr/Ca ratios (especially the former), therefore, is very useful for reconstructing movements of wild-caught Z. dunckeri between not only estuarine and marine habitats, but also mesohaline and polyhaline areas in the study site, during their life histories. According to the results of the rearing water elemental analysis, it appeared that otolith Li/ Ca and Sr/Ca ratios of reared individuals were affected by ambient elemental concentrations rather than ambient element/Ca, because ambient Li/Ca did not differ between 15 and 25 psu, and ambient Sr/Ca was higher in 25 psu compared with 32 psu (Table 2). Similar findings have been reported for other fish species, including galaxiids and latids [26, 37]. The majority of wild-caught Z. dunckeri had relatively invariable Li/Ca and Sr/Ca ratios along the entire otolith transect which remained within the estuarine ranges, suggesting that this species spends its entire life within an estuary (i.e., estuarine resident). Such otolith elemental signatures, however, differed between upstream- and
downstream-dwelling individuals. The former had consistently lower Li/Ca ratios within the estuarine range, indicating an entire life-history within low-salinity areas, such as the upstream station, without movement to the marine environment. In type 1 downstream fish, Li/Ca and Sr/Ca ratios along the otolith transect were mostly within the estuarine ranges, being similar to those of the upstream fish. However, otolith Li/Ca ratios of type 1 fish were higher compared with the upstream fish, some type 1 individuals having temporally spiked values beyond the estuarine range. These results suggested that many type 1 fish spend their entire life in mid- to high-salinity estuaries, although some individuals may be accidentally flushed out of the estuary into the sea, probably due to their weak swimming ability. Heavy flood events may transport them to coastal marine areas, such as the inner bay at the present study site, such individuals immediately returning to estuarine habitats during flood tides [38]. Type 2 fish (28 %), on the other hand, showed otolith Li/Ca and Sr/Ca ratios successively higher than the estuarine ranges in the middle transect section, suggesting that such individuals
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were transferred to and spent a significant period of time (ca. 20 days according to the daily increment analysis of otoliths) in marine areas before returning to estuaries, although no conspecifics were observed around the marine bay station during the study period. The reason why type 2 fish did not return quickly to the estuary is unknown. In summary, the present study explored habitat use patterns of Z. dunckeri by evaluating otolith Li/Ca and Sr/ Ca, suggesting that the species is essentially an estuarine resident, completing its life cycle within an estuarine system, although some individuals may be accidentally washed out of the estuary into the sea. In addition, a multitrace element approach, such as using both otolith Li/Ca and Sr/Ca, may be useful for detecting fish movements between estuarine and marine habitats, and across a finer salinity gradient within an estuary. Acknowledgments We are grateful to Ken Sakihara, Akira Mizutani and the Okinawa Regional Research Center, Tokai University, for assistance with the fieldwork. Constructive comments on the manuscript from Kotaro Shirai, Ken Okamoto, Shigeru Aoki, Graham Hardy and two anonymous reviewers were much appreciated. This study was supported by a GCOE Asian Conservation Ecology between Kyusyu University and the University of Tokyo and a Grantin-Aid for Scientific Research (A) from the Japan Society for the Promotion of Science (No. 26252027).
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