Juvenile fish assemblages in the Jinju Bay region, Korea

Samples were collected at two stations in waters inside and outside Jinju Bay, approximately 15 km apart (Fig. 1). Jinju Bay is shallow and heavily affected by coastal waters, while outside the bay the waters are deeper and less affected by coastal waters and freshwater flows from the Nam River Dam. The two sampling stations were classified according to adjacent geographic features and their distance from the Nam River (Kim et al. 2010; Kang et al. 2011). The inside station was located at the lower reaches of Nam River, surrounded by villages, inlands, islands, and reefs, while the outside station was exposed to open ocean from the southeastern inlet (Fig. 1).

Fig. 1. Location of the stations inside and outside of Jinju Bay, Korea

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Fish samples were collected using a small beam trawl (beam length 6 m; vertical net opening 1 m; mesh size 20 mm) monthly from December 2014 to November 2015 at both stations, with the exception of February 2015, where collection was not possible. The net was towed at a speed of 1.6–1.8 knots for 60 min (daytime). Immediately after capture, fish samples were snap frozen to – 20 °C then taken to the laboratory at Pukyong National University. Once at the laboratory, the total length (TL) of each fish was measured to the nearest millimetre. Bottom water temperature and salinity measurements were also taken monthly using a conductivity-temperature-depth (CTD) metre (SBE-19 plus, Sea-Bird Electronics, Inc.). The CTD metre was also used to measure the depth of the two stations.

All fish species were identified to the lowest possible taxonomic classification according to Kim et al. (2005) and Nakabo (2013). The scientific names and taxonomic classifications of fishes followed Nelson et al. (2016) and Kim and Ryu (2016). And the species collected according to Elliott and Dewailly (1995) were classified into six types according to purpose: estuarine residents (ER), marine adventitious visitors (MA), diadromous (catadromous/anadromous) migrants (CA), and marine seasonal. migrants (MS), marine juvenile migrants (nursery species) (MJ), or freshwater adventitious visitors (FW). The total length and wet body weight of each individual was measured to the nearest millimetre and gram, respectively. The abundance of each species was obtained using the swept area method (number of individuals per km²). Species occurring more than six times (over 50%) during the survey period were considered resident species.

A one-way ANOVA followed by a post hoc Bonferroni’s test, with sample site and season as fixed factors, was used to analyse the abundance data. All species were considered in the analyses, and abundances were log(x + 1) transformed. For the eight most numerically abundant species (comprising greater than 6.0% of the total population), variations in seasonal [spring (March–May), summer (June–August), autumn (September–November), and winter (December–February)] mean abundance were analysed.

A Mann-Whitney U test was used to examine differences in the number of fish species collected from inside and outside Jinju Bay. The community-level variable of fish assemblage was expressed as a species diversity index (H', Shannon and Weaver 1949) using the number of species and its abundance data. A Bray–Curtis similarity matrix was constructed based on the abundance of the fish species (Bray and Curtis 1957). Before calculation, a logarithmic transformation [log₁₀(x + 1)] was applied to the data to decrease the effects of a few but extremely abundant species. Cluster analysis was carried out using the Bray–Curtis similarity. A similarity percentage (SIMPER) was then used to examine which species contributed most to the differences among samples. A non-metric multidimensional scaling (nMDS) ordination was further visualized to examine the cluster relationship on a two-dimensional plot. All multivariate analyses were performed using PRIMER statistical package version 6.0 (Clarke and Gorley 2006).

In addition, relationships between fish abundance and environmental factors (i.e. water temperature, salinity, depth, water transparency) were analyzed using canonical correspondence analysis (CCA). The relative contributions of environmental variables to the observed differences were assessed using correlation coefficients for relationships between each fish assemblage of common fish species and the canonical axis. To avoid overestimation caused by less frequently occurring species, only those accounting for over 0.5% of the total percentage of abundance (resident fish) were used for this analysis. The test was performed using the package Excel XLSTAT V.7.5.2 (Add-in-software, http://www.xlstat.com). Data were log transformed log(x + 1) prior to analysis.

Depth between the stations differed, with depth inside Jinju Bay measured at 10.6 m and the outside at 18.6 m. Bottom water temperatures showed similar trends between the two stations, with a lower temperature measured during winter than during summer (Fig. 2). The extent of seasonal fluctuations in water temperature were greater at the station inside Jinju Bay (6.1–24.2 °C) than outside (8.1–23.3 °C). The difference in bottom water temperature between the stations was greatest in summer, and there was no significant difference in water temperature between stations in winter (Bonferroni’s test, P > 0.05). Salinities were consistently lower at the station inside the bay than outside throughout the year, with the highest salinity occurring in April 2015 inside and the lowest during July 2015 outside (Fig. 2).

Fig. 2. Monthly variations in the bottom water temperature (a) and salinity (b) from inside (black circle) and outside (open circle) of Jinju Bay

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A total of 534,657 individual fishes per square kilometre (ind./km²), comprising of 81 species and 47 families, were collected at both stations. Of these, 188,585 ind./km² belonging to 63 species and 40 families were collected inside the bay, while 346,072 ind./km² from 65 species and 42 families were caught outside the bay (Table 1).

The number of species was similar between stations, but the number of individuals was considerably higher at the station outside than the one inside the bay. The most dominant species was Nuchequula nuchalis, which occurred at a frequency of 26% inside Jinju Bay and at 27% outside the bay. The next most dominant species inside the bay were Thryssa kammalensis (18%) and Zoarces gillii (16%), and Liparis tanakae (17%) and T. kammalensis (9%) outside the bay.

Forty species of young fishes were caught inside the bay, comprising approximately one third of the total number of individuals inside the bay. Forty-seven species of young fishes were caught outside the bay, comprising 52% of individuals caught, indicating that more various species grow outside of the bay. Juvenile P. cornutus, Z. gillii, and Hemitripterus villosus were commonly collected inside the bay from March to June, while at the station outside Jinju Bay, L. tanakae was commonly caught from March to May and Pennahia argentata from September to November (Tables 2 and 3).

While trends between seasons could not be empirically tested due to the lack of replication in seasonal data, monthly data binned into categories that matched particular seasons in Korea showed some interesting patterns. Difference between these binned data can be used to infer potential seasonal changes. The number of fish species varied from 14 to 31 between the four binned seasons, with the highest values recorded at both stations in winter (Fig. 3a). The mean number of species tended to be high during winter and spring at both stations and lowest during autumn (inside the bay) and summer (outside the bay). Fish abundance varied by temporally peaking in summer inside the bay and autumn outside the bay. Abundance was the lowest inside the bay in autumn and outside the bay in winter (Fig. 3b). Greater fish abundances corresponded with high occurrences of N. nuchalis and T. kammalensis during August (Tables 2 and 3). Diversity indices ranged from 0.98 to 2.63 inside the bay and 1.06 to 2.62 outside the bay. The highest diversities were recorded in winter inside the bay and summer outside the bay (Fig. 3c).

Fig. 3. Monthly variations in the number of species, number of individuals (ind./km²), and diversity index (H') of fish collected inside (black) and outside (white) of Jinju Bay, Korea, from December 2014 to November 2015. Wi = winter, Sp = spring, Su = summer, Au = autumn

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Cluster analysis of the 14 common species indicated that less than 1% of the total abundance of fishes were collected from inside the bay. Species were divided into five groups at a similarity level of 60% (Fig. 4a). Group A consisted of L. tanakae, Z. gillii, Ricuzenius pinetorum, Pholis fangi, Repomucenus valenciennei, and Pholis nebulosi, with a high emergence in spring and winter. Group B consisted of N. nuchalis, P. argentata, Sillago japonica, and Conger myriaster and were collected continuously during the survey period. P. cornutus and Inimicus japonicus collected in abundance in spring and summer formed Group C. T. kammalensis collected in summer comprised Group D, and Cynoglossus robustus collected in autumn comprised Group E (Fig. 4b).

Fig. 4. A dendrogram (a) and non-metric multidimensional scaling (nMDS) (b) analysis of fish species collected by beam trawl inside of Jinju Bay, Korea (Nn, Nuchequula nuchalis; Tk, Thryssa kammalensis; Lt, Liparis tanakae; Zg, Zoarces gillii; Pa, Pennahia argentata; Rp, Ricuzenius pinetorum; Pf, Pholis fangi; Rv, Repomucenus valenciennei; Pc, Pleuronichthys cornutus; Sj, Sillago japonica; Cm, Conger myriaster; Cr, Cynoglossus robustus; Pn, Pholis nebulosa; Ij, Inimicus japonicus)

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Common fish species collected outside the bay were divided into four groups at a similarity level of 60% (Fig. 5a). Amblychaeturichthys hexanema, P. argentata, R. valenciennei, S. japonica, Apogon lineatus, Cynoglossus joyneri, and C. interruptuss were caught in high abundance in spring, summer, and autumn and clustered into Group A. L. tanakae, Z. gillii, P. fangi, and Cynoglossus abbreviatus collected in spring and winter formed Group B. Group C comprised of N. nuchalis and T. kammalensis that concentrated in spring and autumn. R. pinetorum collected in the winter formed Group D (Fig. 5b).

Fig. 5. A dendrogram (a) and non-metric multidimensional scaling (nMDS) (b) analysis of fish species collected by beam trawl outside of Jinju Bay, Korea (Nn, Nuchequula nuchalis; Tk, Thryssa kammalensis; Lt, Liparis tanakae; Zg, Zoarces gillii; Ah, Amblychaeturichthys hexanema; Pa, Pennahia argentata; Rp, Ricuzenius pinetorum; Pf, Pholis fangi; Rv, Repomucenus valenciennei; Sj, Sillago japonica; Al, Apogon lineatus; Cj, Cynoglossus joyneri; Ci, Cynoglossus interruptus; Ca, Cynoglossus abbreviatus)

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A canonical correspondence analysis revealed that three environmental factors contributed to fish assemblages between stations, and among common fish species in each of the four seasons (Fig. 6). Differences in fish assemblages between stations were linked to depth and salinity during winter, spring, and autumn, while temperature and depth contributed to differences in fish assemblages during summer (Fig. 6). Among the common fish species, N. nuchalis appeared negatively affected by salinity and depth in spring, summer, and autumn, but not in winter. P. cornutus appeared positively affected by water temperature in all seasons but autumn. T. kammalensis appeared positively affected by water temperature in summer and autumn, but was negatively affected by water temperature in spring.

Fig. 6. Canonical correspondence analysis (CCA) ordination diagrams of stations in relation to environmental variables (temperature, salinity, depth) for young fish species inside (black circle) and outside (white circle) of Jinju Bay, Korea (Species codes are Ap, Acentrogobius pflaumi; Ah, Amblychaeturichthys hexanema; Al, Apogon lineatus; Cs, Chelidonichthys spinosus; Cm, Conger myriaster; Ca, Cynoglossus abbreviatus; Ci, Cynoglossus interruptus; Cj, Cynoglossus joyneri; Cr, Cynoglossus robustus; Hv, Hemitripterus villosus; Hr, Hypodytes rubripinnis; Ij, Inimicus japonicus; Nn, Nuchequula nuchalis; Lt, Liparis tanakae; Ok, Okamejei kenojei; Ps, Parapercis sexfasciata; Pa, Pennahia argentata; Pf, Pholis fangi; Pn, Pholis nebulosa; Py, Pseudopleuronectes yokohamae; Pc, Pleuronichthys cornutus; Pp, Pseudorhombus pentophthalmus; Rv, Repomucenus valenciennei; Rp, Ricuzenius pinetorum; Sj, Sillago japonica; Tk, Thryssa kammalensis; Tt, Tridentiger trigonocephalus; Zg, Zoarces gillii)

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In spring and autumn, the dominant species of fish at both stations were Z. gillii and N. nuchalis. However, the dominant species differed between stations in winter and summer. Pleuronichthys cornutus and N. nuchalis dominated inside the bay, while L. tanakae and T. kammalensis dominated outside the bay.

N. nuchalis occurred in low numbers at both stations in winter, but although the population increased rapidly inside the bay in the summer and outside the bay in autumn, there was no significant difference between the stations (ANOVA, P = 0.29; Fig. 7a). T. kammalensis showed a rapidly increasing trend inside the bay in the summer and was collected in large numbers in both summer and autumn outside the bay (Fig. 7b). Z. gillii and Pholis fangi were intensively collected inside and outside the bay in the spring (Fig. 7c, d). Pleuronichthys cornutus was collected in significantly higher numbers inside of the bay in spring compared to the other seasons (Bonferroni’s test, P < 0.05; Fig. 7e). L. tanakae was collected consistently outside the bay (ANOVA, P = 0.34; Fig. 7f). Amblychaeturichthys hexanema was collected in abundance inside the bay in winter and outside the bay in spring and autumn (ANOVA, P = 0.20; Fig. 7 g). Pennahia argentata was collected consistently outside the bay in summer and autumn (ANOVA, P = 0.14; Fig. 7h).

Fig. 7. Seasonal variations in mean abundance of 8 common fish species (a–h) between inside (black stick) and outside (white stick) of Jinju Bay, Korea, from December 2014 to November 2015

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Juvenile P. cornutus, Z. gillii, H. villosus, L. tanakae, and P. argentata were collected inside and outside the bay (Fig. 8). P. cornutus occurred during seven of the monthly surveys (March–September) at both stations. These fish exhibited average lengths of 4.7 cm ± 0.5 cm (± SD) in March and 17.3 cm ± 1.1 cm in September. Z. gillii was collected over 3 months (April–June) inside the bay and over 4 months (April–July) outside the bay. H. villosus occurred over 3 months (March–May) inside the bay and for 2 months (March–April) outside the bay. These three species were collected more frequently from inside than from outside of the bay (Fig. 8). On the other hand, L. tanakae was found inside (6.2–18.5 cm TL) and outside (8.1–12.2 cm TL) of the bay over 3 months (March–May), but more individuals were collected at the station outside the bay than inside the bay. In addition, P. argentata (inside bay, 4.1–14.8 cm TL; outside of bay, 5.7–15.8 cm TL) were found more frequently outside the bay than inside, over 3 months (September–November). Xenocephalus elongatus occurred over 2 months (October–November), but only outside the bay. All of these species were collected continuously throughout the study period, with TL increasing steadily over time, suggesting that these fish belonged to a single generation (Fig. 8).

Fig. 8. Monthly change in length-frequency distribution of the six species caught with a beam trawl inside (black stick) and outside (white stick) of Jinju Bay, Korea, from December 2014 to November 2015

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