Corresponding author: Jian Yang ( jiany@ffrc.cn ) Academic editor: Adnan Tokaç
© 2021 Ying Xiong, Jian Yang, Tao Jiang, Hongbo Liu, Xiaming Zhong.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Xiong Y, Yang J, Jiang T, Liu H, Zhong X (2021) Temporal stability in the otolith Sr:Ca ratio of the yellow croaker, Larimichthys polyactis (Actinopterygii, Perciformes, Sciaenidae), from the southern Yellow Sea. Acta Ichthyologica et Piscatoria 51(1): 59-65. https://doi.org/10.3897/aiep.51.63245
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Otolith chemical signatures are sufficiently stable across time to allow for accurate stock classification. The classification of the southern Yellow Sea population for Larimichthys polyactis (Bleeker, 1877) and its connectivity with others from 1962 is controversial. The study aimed to study the inter-annual variation in otolith strontium:calcium (Sr:Ca) ratios of L. polyactis to determine whether otolith natural tags are representative over long periods and can then be used for population structure classification. Spawning L. polyactis individuals were captured by stow nets in the same site of the southern Yellow Sea coastal waters during April–May in 2003, 2012, and 2013. EPMA (electron probe microanalysis) was used to determine the Sr:Ca ratios of a total of 25 otolith samples. Mann–Whitney U-test was used to test the differences of otolith Sr:Ca ratios from the core to edge for each otolith. One-way ANOVA was performed to compare the mean otolith Sr:Ca values among 2003, 2012, and 2013. Otoliths from 2003, 2012, and 2013 showed similar patterns of Sr:Ca ratios and Sr:Ca ratios could be divided into higher and lower phases in the core and remaining regions, respectively. Inter-annual significant differences for each high or low Sr:Ca phase of otoliths were not observed over short- (between 2012 and 2013) or long-time (between 2003 and 2012, and between 2003 and 2013) scales. Univariate contrasts across the adjacent year and decade classes were statistically similar. The Sr:Ca ratio signatures in the otolith were relatively stable across years and can be used as a reliable natural tag for connectivity assessments and stock identification with little or no genetic differentiation among L. polyactis populations. The short- and long-term temporal stability of otolith Sr:Ca ratios also revealed, the existence of stable L. polyactis stocks in the southern Yellow Sea, consistent with a previous finding of capture survey.
Larimichthys polyactis, southern Yellow Sea, Sr:Ca ratio, temporal stability
Otoliths are used as natural tags in fish, because of their capacity to record time-resolved lifetime environmental histories, which provides an opportunity for geolocating individual fish in time and space (
The yellow croaker, Larimichthys polyactis (Bleeker, 1877) (Perciformes: Sciaenidae), is an important fish species endemic to the Northwest Pacific, inhabiting coastal waters across the Yellow, Bohai, and East China seas (
The otolith strontium:calcium (Sr:Ca) ratio of concentrations have been applied as a useful scalar to estimate habitat use, migration history, and distinguish population structures of fish (
Spawning L. polyactis individuals were captured by stow nets in the southern Yellow Sea coastal waters (Fig.
High and low phases of the strontium:calcium (Sr:Ca) ratio in Larimichthys polyactis otoliths. High and low phases of the Sr:Ca ratio in Larimichthys polyactis otoliths collected in 2003, 2012, and 2013.
Year | Sample code | Standard | Estimated | High Sr:Ca phase | Low Sr:Ca phase | ||
---|---|---|---|---|---|---|---|
length [mm] | age | Distance from the core [μm] | Sr:Ca | Distance from the core [μm] | Sr:Ca | ||
(mean ± SD) | (mean ± SD) | ||||||
2003 | LSPP12 | 134 | 1+ | 0–240 | 7.57 ± 1.20 a | 260–3,180 | 5.77 ± 0.80 b |
LSPP13 | 136 | 1+ | 0–140 | 6.97 ± 0.73 a | 160–2,180 | 4.60 ± 0.74 b | |
LSPP14 | 148 | 1+ | 0–140 | 7.16 ± 1.51 a | 160–2,500 | 4.74 ± 0.63 b | |
LSPP15 | 141 | 1+ | 0–180 | 7.10 ± 1.16 a | 200–2,100 | 4.71 ± 0.78 b | |
LSPP18 | 162 | 1+ | 0–40 | 7.68 ± 1.50 a | 60–3,040 | 4.31 ± 0.80 b | |
LSPP19 | 161 | 1+ | 0–200 | 6.85 ± 1.24 a | 220–4,260 | 4.76 ± 0.99 b | |
LSPP20 | 183 | 2+ | 0–160 | 6.90 ± 0.96 a | 180–1,900 | 4.88 ± 0.78 b | |
LSPP21 | 141 | 1+ | 0–300 | 7.64 ± 0.95 a | 320–2,320 | 5.48 ± 0.92 b | |
2012 | LSPP01 | 156 | 1+ | 0–200 | 7.67 ± 1.03a | 220–3,300 | 4.31 ± 0.88b |
LSPP02 | 106 | 1+ | 0–280 | 7.31 ± 0.59 a | 300–2,480 | 5.18 ± 0.92 b | |
LSPP03 | 115 | 1+ | 0–80 | 7.02 ± 2.36 a | 100–3,280 | 4.69 ± 1.01 b | |
LSPP04 | 117 | 1+ | 0–160 | 6.63 ± 0.58 a | 180–2,760 | 4.60 ± 0.96 b | |
LSPP05 | 109 | 1+ | 0–180 | 7.04 ± 1.09 a | 200–2,940 | 5.33 ± 0.92 b | |
LSPP06 | 122 | 1+ | 0–60 | 6.68 ± 0.26 a | 80–3,140 | 4.82 ± 0.95 b | |
LSPP07 | 107 | 1+ | 0–60 | 7.74 ± 1.46 a | 80–3,440 | 4.73 ± 0.86 b | |
LSPP08 | 118 | 1+ | 0–300 | 7.58 ± 0.88 a | 320–3,420 | 4.36 ± 0.98b | |
LSPP09 | 123 | 1+ | 0–240 | 7.14 ± 0.83 a | 260–3,340 | 4.85 ± 1.00 b | |
LSPP10 | 112 | 1+ | 0–380 | 6.40 ± 0.64 a | 400–2,780 | 5.16 ± 1.09b | |
2013 | LSLP02 | 138 | 1+ | 0–80 | 7.62 ± 1.17 a | 100–3,480 | 4.28 ± 0.81 b |
LSLP04 | 186 | 2+ | 0–220 | 7.18 ± 1.17 a | 240–2,520 | 4.76 ± 0.81 b | |
LSLP05 | 152 | 1+ | 0–80 | 7.55 ± 1.94 a | 100–4,340 | 4.77 ± 0.90 b | |
LSLP07 | 122 | 1+ | 0–160 | 6.79 ± 1.14 a | 180–2,020 | 4.57 ± 0.85 b | |
LSLP08 | 143 | 1+ | 0–80 | 7.75 ± 1.10 a | 100–2,760 | 5.09 ± 0.92 b | |
LSLP09 | 133 | 1+ | 0–120 | 7.61 ± 1.30 a | 140–2,200 | 4.42 ± 1.02 b | |
LSLP10 | 151 | 1+ | 0–80 | 7.34 ± 1.43 a | 100–1,980 | 4.48 ± 0.86 b |
Methods of preparing L. polyactis otoliths for use in electron probe microanalysis (EPMA) measurement have been described by
EPMA was used to study the Sr and Ca concentrations, based on the method described by
Based on our previous study in 2012, which was the first time L. polyactis otoliths from the southern Yellow Sea were analyzed (
X-ray intensity map of strontium (Sr) content and strontium:calcium (Sr:Ca) ratios fluctuation in Larimichthys polyactis otolith. X-ray intensity map of the Sr content in Larimichthys polyactis otoliths collected in 2012 from the southern Yellow Sea (left). This pattern is representative of with overall low Sr levels (greenish and yellowish color), except for higher Sr contents in the core (reddish color). Mean Sr:Ca ratios fluctuated (with positive SD values) along the transect from the core (0 μm) to the edge of otoliths (right). The figure in 2012 has been referenced from
Comparison for high and low strontium:calcium (Sr:Ca) phases in Larimichthys polyactis otoliths. One-way ANOVA results for high Sr:Ca and low Sr:Ca phases in Larimichthys polyactis otoliths compared in 2003, 2012, and 2013.
MS | df | F | P | Significance level | ||
---|---|---|---|---|---|---|
High Sr:Ca phase | Inter-groups | 0.167 | 2 | 1.082 | 0.356 | NS |
Within-groups | 0.154 | 22 | ||||
Low Sr:Ca phase | Inter-groups | 0.151 | 2 | 1.070 | 0.360 | NS |
Within-groups | 0.141 | 22 |
According to L. polyactis baseline data from 2012 (
where X and Y represent two samples (high and low phases) in this study, and m and n are their sample sizes, respectively.
Unlike the Mann–Whitney U-test, which compares median values between two groups, one-way ANOVA compares values among multiple sets of groups. In this study, one-way ANOVA was used to determine whether the otolith Sr:Ca values varied with time for three comparisons across an adjacent year (2012 vs. 2013) and decade (2003 vs. 2012, and 2003 vs. 2013), calculated from the high and low Sr:Ca phases, respectively. The assumption of normality and homogeneity of variance for each variable was examined using Kolmogorov–Smirnov (KS) and Levene’s tests, and the variables were log-transformed if necessary. Variables that did not pass the normality and homogeneity tests were excluded from further analysis. Statistical analysis was performed using IBM SPSS (version 19.0; IBM Corp., Armonk, NY, USA).
One-way ANOVA was defined as:
where SSB represents the sum of squares between groups, SSW represents the sum of squares within-group, MSB represents the mean square between groups, MSW represents the mean square within-group, VB represents the degrees of freedom between-groups (VB = 2), VW represents the degrees of freedom within-group (VW = 22) , i represents three groups (2003, 2012, and 2013), and j represents the total number of samples (n = 25) minus K (3 groups), namely 22.
The age of each sample of the presently reported study was estimated with the body length-at-age growth equation
reported by
Otoliths from 2003, 2012, and 2013 showed similar patterns of Sr:Ca ratios (Table
The mean Sr:Ca ratios of the regions in the high Sr:Ca phase ranged from 6.79 to 7.68 in 2003, 2013, and 2012, whereas the corresponding ratios in the low Sr:Ca phase varied substantially in the remaining stages (Fig.
Inter-annual differences in otolith chemistry were not observed over short- (between 2012 and 2013) or long-time (between 2003 and 2012, and between 2003 and 2013) scales (Table
In the presently reported study, the L. polyactis otolith Sr:Ca ratios were the highest and most variable near the otolith core in 2003, 2012, and 2013, which was possibly influenced by ontogenetic physiology and ambient chemistry. High Sr in the adult stage is more likely to reflect physiological state, particularly reproduction, than to reflect waterborne sources (
In L. polyactis later developmental stages, the otolith Sr:Ca ratios remained stable and showed no significant differences between short- and long-time, suggesting that this ontogenetic stage experienced a relatively uniform physicochemical environment, which is supported by the fact that Ca and Sr exhibit quasi-conservative distributions resulting in comparatively stable Sr:Ca levels (
The Sr:Ca ratio was selected to infer migration through habitats with different salinities in otolith microchemistry studies. Otolith Sr:Ca from Pangasius krempfi Fang et Chaux, 1949 varied between 1999 and 2017, possibly owing to changes in water environmental conditions with the development of hydropower dams along the Mekong River (
Furthermore, we documented directly, for the first time, the uniform migratory history demonstrated by stable Sr:Ca over short- and long-term scales, which could suggest the existence of a stable L. polyactis stock in the southern Yellow Sea. This corroborates the findings of a previous fishery investigation during 2003 and 2013 that showed a similar migration distribution for L. polyactis in the southern Yellow Sea (
In conclusion, the L. polyactis otolith Sr:Ca signatures were found to be stable across years in the southern Yellow Sea, and therefore we suggest that further studies on L. polyactis should focus on the connectivity of spawning groups and overwintering groups, and their population structure in China seawater by analyzing the otolith microchemistry.
This study was supported by the National Natural Science Foundation of China (Grant No. 31802297).