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Article

Comparison of Abundance and Structure of Larval Fish Assemblages between Autumn and Spring in the Waters Surrounding Taiwan Bank, Western North Pacific

by
Hung-Yen Hsieh
1,*,
Ming-An Lee
2,3,
Wei-Lun Chiu
1 and
Pei-Jie Meng
1,4,*
1
Graduate Institute of Marine Biology, National Dong Hwa University, Pingtung 94450, Taiwan
2
Department of Environmental Biology and Fishery Science, National Taiwan Ocean University, Keelung 20224, Taiwan
3
Center of Excellence for Ocean Engineering, National Taiwan Ocean University, Keelung 20224, Taiwan
4
Taiwan Ocean Research Institute, Kaohsiung City 852, Taiwan
*
Authors to whom correspondence should be addressed.
Fishes 2024, 9(1), 16; https://doi.org/10.3390/fishes9010016
Submission received: 4 December 2023 / Revised: 25 December 2023 / Accepted: 27 December 2023 / Published: 29 December 2023
(This article belongs to the Section Biology and Ecology)
Browse Figures
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Abstract

:
The fluctuations in both time and space of larval fish assemblages in relation to hydrographic characteristics in the waters surrounding Taiwan Bank were studied in October 2021 (autumn) and March 2022 (spring). Throughout the study period, we identified a total of 149 taxa of fish larvae, encompassing 96 genera and 71 families. Engraulis japonicus, Diaphus slender type, unidentified Gobiidae, Apogon sp., unidentified Clupeidae, and Benthosema pterotum were the six dominant taxa and together constituted 47.39% of the total catch. There were no notable temporal variations observed in the abundance of fish larvae, but the species number of fish larvae was greater in spring than in autumn. Significant variations in species composition were observed between the different cruises, and the cluster analysis unveiled a distinct temporal structure of the assemblages of fish larvae. The dynamics of the prevailing currents induced by seasonal monsoons contribute significantly to the transportation of fish larvae. The distribution of fish larvae showed a good association with hydrographic characteristics, where seawater temperature and salinity emerged as the primary explanatory factors influencing the composition of larval fish assemblages in the waters surrounding Taiwan Bank. While the increased influx of nutrients from upwelling ensures abundant food availability, the hydrographic conditions may not be suitable for every fish larva.
Keywords:
topographic upwelling; currents; seasonal monsoons; larval dispersal; Taiwan Strait
Key Contribution: Seasonal monsoon-driven currents play a crucial role in the transportation of fish larvae. The relationship observed between hydrographic variables and larval fish assemblages further suggests the possible use of these assemblages as tracers for surface circulation in the waters surrounding Taiwan Bank. The present study not only enhances our understanding of ecosystems in the region but also provides good examples of biotic responses to hydrographic conditions and interactions among water masses.

1. Introduction

The composition of larval fish assemblages arises from the convergent spawning strategies employed by various species, capitalizing on favorable environmental conditions to enhance larval survival [1,2]. In continental shelf waters characterized by tropical and subtropical climates, the distribution pattern of larval fish assemblages is complex [3,4,5]. As a result of the initial developmental stages occurring in the planktonic environment in the fish life cycle, their development is influenced by a combination of physical factors, including temperature, salinity, and currents, as well as biological factors, like food availability and predator stocks [5,6]. The variability in these processes directly or indirectly impacts the distribution and survival of fish larvae, resulting in significant fluctuations in the annual recruitment of species [7]. Thus, the connection between larval fish assemblages and physical–biological processes is gaining greater significance in the context of the management of fisheries based on ecosystem considerations and assessments of fish stocks independent of fishing activities [5,6].
The Taiwan Strait, situated between mainland China and the island of Taiwan, is a shallow channel (~60 m) of 350 km in length and 180 km in width. It serves as a crucial link connecting the East China Sea (ECS) and the South China Sea (SCS), playing a significant role in the exchange of biota between these two seas. The Taiwan Strait experiences pronounced seasonal variations in currents, primarily influenced by the East Asian monsoon system and the underwater topography (bathymetric features) [8,9]. In this region, there are three primary currents: (i) the cold, low-salinity, and nutrient-rich China Coastal Current (CCC), (ii) the warm and low-salinity South China Sea Warm Current (SCSC), and (iii) the warm, high-salinity, and oligotrophic Kuroshio Branch Current (KBC). In the cold season, when the northeastern monsoon is predominant, the CCC flows in a southward direction along the coast of mainland China and into the central Taiwan Strait. Simultaneously, the KBC courses through the Luzon Strait, extending into the northern SCS and the southeastern Taiwan Strait [8,10]. As the northeastern monsoon weakens and transitions into the southwestern monsoon in late spring, the SCSC gradually displaces the KBC, flowing in a northward direction into the northern Taiwan Strait [8,9].
The bathymetric topography in the Taiwan Strait is complex. It consists of a shallow shelf bordering the coast of China, the Chang-Yuen Ridge, Taiwan Bank, and the Penghu Channel [11]. Among these topographies, Taiwan Bank, located in the southern region of the Taiwan Strait, is characterized by sand dunes, with an average water depth of approximately 20 m. The formation of an upwelling area may have different mechanisms. As reported by Tang et al. [12] and Hu et al. [13], multiple upwelling regions have been recognized in the Taiwan Strait, with one notable example being the Taiwan Bank Upwelling. The Taiwan Bank Upwelling (Figure 1), characterized by a banana-shaped area covering approximately 2500–3000 km2 and located close to the southern perimeter of Taiwan Bank, occurs consistently throughout the year, primarily in summer, exhibiting variable strength and scale [12,13,14]. This upwelling region stands as the primary fishing ground in the Taiwan Strait for stick-held dip-net fishing, pole and line, longline fishing, and gillnet fisheries.
While upwelling regions make up just 0.1% of the world’s oceans, their significance in fishery production is noteworthy, contributing to nearly half of the world’s total fishery production [15,16]. Therefore, a good understanding of hydrographic and biological variations is essential for fish production and further resource management. In the Taiwan Strait, Hsieh et al. [17] examined the composition of larval fish assemblages during various monsoon periods from 2003 to 2004. They suggested that the crucial factor influencing the dispersion and assemblage composition of larval fish is the cyclical intrusion of currents in the Taiwan Strait propelled by seasonal monsoons. Furthermore, the turbulence caused by the winter front and local topographic upwelling play a role in enhancing biological production. This, in turn, leads to elevated concentrations of chlorophyll a and increased zooplankton biomass, providing ample food resources crucial for the survival of larval fish. However, according to Lee et al. [18], the Taiwan Strait has consistently experienced warming trends attributable to the impact of climate change since 1919. In 2020, the seawater temperature in the Taiwan Strait was notably 2 °C higher than the average seawater temperature recorded in the 1980s. We thought that the strength of the upwelling force in the area and its surrounding environment could be modified as a result of the effects of climate change. Therefore, we were interested in investigating whether there had been any changes in the assemblage of fish larvae in this study area over the past two decades. The study aimed to (i) contrast the taxonomic compositions, abundance, and assemblages of fish larvae in the waters surrounding Taiwan Bank during autumn and spring and (ii) assess the impact of monsoon-driven currents and topographic upwelling on the distribution patterns of larval fish assemblages. The contrasting hydrographic conditions in the waters surrounding Taiwan Bank during autumn and spring led us to hypothesize that the distinct marine environment variations result in different assemblages of fish larvae in these two seasons.

2. Materials and Methods

2.1. Oceanographic and Biological Sampling

Two cruises of the R/V New Ocean Researcher 3 in the waters surrounding Taiwan Bank were carried out during 19–21 October 2021 (hereafter autumn) and 8–11 March 2022 (hereafter spring) (Figure 2). Zooplankton samples were collected during both the autumn and spring cruises, in the day and at night, at eight and ten stations, respectively. An Ocean Research Institute (ORI) net, measuring 6 m in length, with a 1.6 m mouth diameter and a 330 μm mesh size, was employed for collection. The net was vertically towed at a velocity of around 1 m s−1, commencing from a depth of 200 m (at stations with a depth of less than 210 m, the net was towed starting from a depth of 10 m above the bottom) and extending up to the surface. The volume of filtered water was estimated by employing a flowmeter (Hydro-Bios, Kiel, Schleswig-Holstein, Germany) installed at the center of the net. The filtered water volume at each station ranged from 125 to 1036 m3. Upon being brought back from the ocean, the zooplankton samples were promptly preserved through immersion in a solution consisting of 5% buffered formalin and seawater. Before collecting zooplankton at each station, vertical profiles of temperature, salinity, and fluorescence were acquired using a General Oceanic SeaBird CTD (SEB-911 plus; Bellevue, Washington, DC, USA), covering the range from the surface to 10 m above the bottom.

2.2. Identification and Enumeration

In the laboratory, the zooplankton samples were split into two portions using a Folsom plankton splitter, a device by Aquatic Research Instruments, Wellington, New Zealand. From one randomly chosen subsample, fish larvae were sorted and then preserved in 95% alcohol following the sorting procedure. The fish larvae were identified to the most specific taxonomic level achievable, relying on their morphological characteristics in accordance with Okiyama [19], Leis and Trnski [20], and Chiu [21]. The second subsample was successively divided until the final subsample reached a range of 1000–2000 or fewer. The aforementioned subsample was then employed to compute the abundance of zooplankton. Larval fish and zooplankton abundance values were measured in terms of individuals per 1000 m3 and 1 m3, respectively.

2.3. Statistical Analyses

Temperature and salinity vertical profiles within the upper 50 m were depicted with the utilization of SURFER 8.01 software, developed by Golden Software, Inc., based in Golden, CO, USA. To analyze temporal fluctuations in species diversity and relative abundance of species in an assemblage, calculations were performed for the Shannon–Wiener diversity index (H′) [22] and Pielou index of evenness (J′) [23]. The differences in hydrographic variables between the cruises were examined using one-way ANOVA [24]. The non-parametric Mann–Whitney U-test [25] was employed to ascertain the significance of distinctions in zooplankton abundance and of the abundance and diversity of fish larvae between the different cruises. To examine temporal and spatial variations in the larval fish assemblages, PRIMER version 6 (PRIMER-E, West Hoe, Plymouth, UK) was utilized for our analysis using multivariate statistical methods. Before conducting the analysis, data on larval fish abundance (those constituting > 1% of the total larval catch) were log (x + 1)-transformed to mitigate the influence of dominant taxa, following the approach outlined by Clarke and Warwick [26]. A triangular similarity matrix among sampling stations, used to generate a cluster dendrogram, was built using Bray–Curtis similarities [27]. In the meantime, non-metric multi-dimensional scaling (MDS) [28] was employed to produce a two-dimensional visual depiction of the assemblage structure. The similarity percentage routine (SIMPER) [29] was utilized to illustrate how each taxon contributed to the average similarities within diverse larval fish assemblages, showing their percentage contribution. Moreover, distance-based linear models (DistLM, a component of the multivariate statistical software PERMANOVA+ for PRIMER version 6) [30] were selected to assess the connection between hydrographic variables and larval fish assemblages. Constructed through the stepwise selection procedure, these models utilized adjusted R2 as the criterion for selection. Ultimately, the entire model was depicted through an examination of the ordination from distance-based redundancy analysis (dbRDA) [31].

3. Results

3.1. Hydrographic and Biological Conditions

The seawater at a 10 m depth in the waters surrounding Taiwan Bank showed a clear temporal change in temperature (one-way ANOVA, F = 53.067, p < 0.001). A higher mean value of temperature was observed in autumn than in spring (Table 1). In autumn, the temperature ranged from 26.86 °C to 28.94 °C, while in spring, it ranged from 20.11 °C to 24.80 °C. The examination of the temperature vertical profiles indicated that in both cruises, the water column exhibited thorough vertical mixing (Figure 3). When considering the entire study area, the isotherm distribution pattern revealed a gradient running from northwest to southeast, with temperatures gradually rising from high to low latitudes, notably during spring (20 to 25 °C).
During autumn, seawater salinity varied between 33.91 and 34.05, while in spring, it fluctuated within the range of 33.79 to 34.33. A distinct difference in salinity between the cruises was observed (Table 1), with significantly higher salinity being recorded in spring than in autumn (one-way ANOVA, F = 8.824, p < 0.01). Salinity values were generally lower in the southern Taiwan Bank in autumn, such as at stations B7, B32, and B33; on the contrary, slightly lower salinity values were recorded in the northern Taiwan Bank in spring, but no significant spatial difference was observed (Figure 3).
Fluorescence showed no significant temporal difference (one-way ANOVA, F = 0.234, p = 0.635). In the study, fluorescence ranged from 0.08 mg m−3 to 1.40 mg m−3 in autumn and from 0.06 mg m−3 to 1.86 mg m−3 in spring. A slightly higher mean value was recorded in spring (Table 1). In general, higher values (>1.00 mg m−3) were found on the northern side of the bank (within or adjacent to an upwelling area), with the highest values being found at stations B10 and B6 for both cruises, respectively.
In autumn, zooplankton abundance ranged from 108 ind. m−3 to 791 ind. m−3, while in spring, it fluctuated between 175 ind. m−3 and 832 ind. m−3. The respective means were 381 ± 227 (SD) ind. m−3 in autumn and 451 ± 226 ind. m−3 in spring. No significant difference in zooplankton abundance was observed between the two cruises (Mann–Whitney U-test, U = 31, p = 0.424). The distribution pattern of zooplankton abundance showed a significant positive correlation with fluorescence (simple regression analysis, F = 5.948, p < 0.05), and zooplankton usually showed higher abundance at stations B6, B10, and B14 (Figure 4).

3.2. Composition of Fish Larvae

The current study collected a total of 1968 larval fish specimens, from which 149 taxa or morphotypes were identified, encompassing 71 families and 96 genera. Among these specimens, a notable portion consisted of unidentified individuals, comprising 2.91% of the total catch. Yolk-sac larvae constituted 6.01% of the total catch, and there were also specimens damaged during collection, accounting for 0.99% of the total catch. The larvae belonging to the families Myctophidae, Engraulidae, Gobiidae, Apogonidae, Clupeidae, and Bregmacerotidae were the most abundant in the study, constituting 23%, 13%, 10%, 7%, 6%, and 5% of the total catch, respectively. Within this collection, Myctophidae exhibited the highest species diversity, with 19 taxa, followed by Gobiidae with 6 taxa, Bregmacerotidae with 3 taxa, Engraulidae with 2 taxa, Apogonidae with 2 taxa, and Clupeidae with 1 taxon. The most frequently captured families (>1% of the total fish larvae) in both cruises are ranked in Table 2. The top five dominant families in autumn were Engraulidae, Gobiidae, Apogonidae, Bregmacerotidae, and Myctophidae; by contrast, the predominant families in spring were Myctophidae, Clupeidae, Ammodytidae, Gobiidae, and Sparidae.
At the species level, Engraulis japonicus constituted 12.71% of the total catch, representing the most abundant taxon during the survey. Diaphus slender type (12.71%), unidentified Gobiidae (7.57%), Apogon sp. (6.77%), unidentified Clupeidae (6.26%), and Benthosema pterotum (5.11%) were the next five most abundant fish larvae. These six taxa together constituted 47.39% of the total larval abundance. During the two cruises, the species compositions of dominant fish larvae differed significantly (Table 3). In autumn, E. japonicus, Apogon sp., unidentified Gobiidae, Bregmaceros sp., unidentified Myctophidae, Tridentiger sp., and Trichiurus lepturus were abundant, accounting for 65.65% of total larval fish numerical abundance. Among these seven taxa, the prevalence of E. japonicus surpassed that of the remaining taxa, reaching its highest abundance at station B10 with a peak of 877 ind. 1000 m−3. In spring, the top five prevailing taxa included Diaphus slender type, unidentified Clupeidae, B. pterotum, Bleekeria mitsukurii, and unidentified Gobiidae, contributing 51.89% to spring total catch. The three dominant taxa, namely, Diaphus slender type, unidentified Clupeidae, and B. pterotum, showed significantly higher abundance at stations B17 (521 ind. 1000 m−3), B14 (442 ind. 1000 m−3), and B6 (163 ind. 1000 m−3), respectively.

3.3. Temporal Changes in Abundance and Diversity of Fish Larvae

The overall mean abundance (mean ± SD) during the study period was 415 ± 358 ind. 1000 m−3, ranging from 97 ind. 1000 m−3 to 1227 ind. 1000 m−3 in autumn and from 29 ind. 1000 m−3 to 1025 ind. 1000 m−3 in spring, respectively. The average abundance of fish larvae showed a slight increase in autumn compared with spring (Table 1). However, it is important to note that no statistically significant difference was observed in the abundance of fish larvae between these two seasons (Mann–Whitney U-test, U = 30, p = 0.374). No distinct distribution difference in abundance was observed for both cruises (Figure 5). Nevertheless, relatively higher abundance of fish larvae occurred at stations B10, B11, and B15 in autumn and at stations B6, B7, B14, and B17 in spring, respectively.
Although the total number of larval fish species in spring exceeded that in autumn (Table 1), there was no significant temporal difference in the species number, as indicated by the Mann–Whitney U-test (U = 31, p = 0.422). In autumn, fish larvae from a total of 37 families, 46 genera, and 66 taxa were identified. The species diversity and evenness of fish larvae in autumn exhibited variability across stations, ranging from 0.86 to 2.78 for species diversity and from 0.44 to 0.89 for species evenness. In contrast to autumn, spring documented 104 taxa, representing 51 families and 61 genera. Species diversity ranged from 0.45 to 2.91, and species evenness fluctuated between 0.55 and 0.93 during spring. Both species diversity (Mann–Whitney U-test, U = 34, p = 0.594) and species evenness (Mann–Whitney U-test, U = 37, p = 0.789) exhibited no statistically significant temporal differences (Table 1). Overall, the distributions of diversity and evenness were consistent with the pattern of species number.

3.4. Assemblages of Fish Larvae

The cluster analysis of Bray–Curtis similarity matrices, using 18 larval fish taxa with relative abundance greater than 1%, produced a dendrogram. This dendrogram defined three station groups at a similarity level of 16%, as illustrated in Figure 6. A clear structure corresponding to the sampling seasons was observed for the assemblages of fish larvae. Table 4 displays the percentage contributions of the dominant taxa within each station group.
Station B10 during spring constituted the exclusive member of Group A, displaying the lowest species number and species diversity (0.45) compared with all other sampling stations. In this group, two larval fish taxa, namely, unidentified Mullidae and Upeneus japonicus, were identified. Both of these taxa belong to coastal and benthic species.
Group B (autumn assemblage) included all autumn stations. Within this station group, the dominant larval fish taxa included Engraulis japonicus, Apogon sp., unidentified Gobiidae, Bregmaceros sp., unidentified Myctophidae, Tridentiger sp., and Trichiurus lepturus. According to the SIMPER routine, the most crucial discriminators (Sim/SD > 1) for this group were identified as unidentified Gobiidae and unidentified Myctophidae (Table 4). In addition, two commercial species, E. japonicus and T. lepturus, were prevalent in this station group, providing contributions of 6.46% and 6.33% to this group, respectively.
Group C (spring assemblage) comprised nine spring stations. Diaphus slender type, unidentified Clupeidae, Benthosema pterotum, Bleekeria mitsukurii, and unidentified Gobiidae were the dominant taxa in this station group. Among them, Diaphus slender type showed the highest abundance of 521 ind. 1000 m−3 at station B17, adjacent to southwestern Taiwan, while unidentified Clupeidae, B. pterotum, B. mitsukurii showed the highest abundance at station B14, with values of 442, 80, and 116 ind. 1000 m−3, respectively. The SIMPER routine identified mesopelagic species B. pterotum as the most important discriminator (Sim/SD > 1) for this group, with a contribution of 36.77% (Table 4). In addition, two commercial species (Trichiurus lepturus and Planiliza sp.) and two coastal species (Cubiceps pauciradiatus and B. mitsukurii) were also significant within this group, collectively contributing 54.98% of the observed patterns.

3.5. Relationship between Environmental Variables and Larval Fish Assemblages

The distance-based linear model was used to examine the relationship between larval fish assemblages and environmental variables. The collective impact of all five environmental variables accounted for 54.56% of the total variation (Table 5). The structure of larval fish assemblages in the waters around Taiwan Bank was significantly influenced by two explanatory variables: seawater temperature (26.76%, p = 0.001) and salinity (13.10%, p = 0.026). These were the only variables found to have a statistically significant impact. In the fitted model, the dbRDA biplot revealed that axes 1 and 2 explained 58.1% and 22.5% of the variance, respectively. These percentages corresponded to 31.6% and 12.3% of the total variance in the original Bray–Curtis similarity matrix (Figure 7). The alterations in larval fish assemblages between the cruises were associated with a decrease in seawater temperature and an increase in salinity.

4. Discussion

The abundance of fish larvae did not exhibit significant temporal variation in the waters surrounding Taiwan Bank. However, there is a notable difference in the composition of larval fish assemblages between autumn and spring. During spring, the KBC transported a higher quantity of mesopelagic fish larvae into this study area.
Variations in the taxonomic composition of larval fish assemblages and the abundance of individual taxa were observed across both space and time in the waters surrounding Taiwan Bank. In this study, the two primary seasonal assemblages of fish larvae were distinct from one another in terms of both the variety of species and the number of individual larvae present. This distinct difference can be attributed to the prevalence of neritic/oceanic–epipelagic species in the autumn assemblage and neritic/mesopelagic species in the spring assemblage. According to the analysis of the prevalent larval fish compositions during the two cruises, aside from the presence of demersal taxon overlap, such as unidentified Gobiidae, the autumn assemblage was defined by Engraulis japonicus, Apogon sp., and Bregmaceros sp. On the other hand, the spring assemblage was primarily led by lanternfishes like Diaphus slender type and Benthosema pterotum, unidentified Clupeidae, and Bleekeria mitsukurii (Table 3). We hypothesized two potential sources to explain the presence of these fish larvae in the waters surrounding Taiwan Bank: (i) the possibility of subtropical coastal fish spawning and hatching within the study area and (ii) the potential origin of oceanic mesopelagic fish larvae from either the KBC or the SCSC. In the following sections, we provide support for the aforementioned speculations with two illustrative examples.
First, Engraulis japonicus was the most abundant taxon in autumn. Engraulis japonicus stands out as one of the most abundant and commercially significant small pelagic fish, frequently found in subtropical-to-temperate waters across the Indo-Pacific region. The harvesting of larval anchovy is a significant economic activity in the coastal regions of Taiwan [32,33]. In the western North Pacific, populations of E. japonicus along coastal areas are distributed from the Korean Peninsula to southeastern China along the continental coast. According to Lee et al. [32] and Tu et al. [34], adults of E. japonicus exhibit a migratory pattern, moving from the East China Sea to the coastal waters of Taiwan, predominantly during the winter and spring seasons for the purpose of spawning. Nevertheless, the appearance of E. japonicus in autumn is surprising, since the predominant currents in the Taiwan Strait typically move in a northerly direction [35]. Remarkably, a comparable increase in E. japonicus larvae during autumn was also noted in the I-lan Bay of northeast Taiwan [36]. A potential explanation is that adults of E. japonicus may migrate southward to reach their spawning grounds along the coast of Mainland China. This movement is particularly notable in autumn when the northerly flow is comparatively weak and less persistent [35].
Secondly, myctophid larvae were dominant in spring. Mesopelagic fish larvae primarily dwell in deeper oceanic waters [37]. These larvae are particularly prevalent in the Kuroshio Current and in offshore oceanic waters [38,39]. In the waters off Japan’s Kuroshio axis and the offshore area to the south, Sassa et al. [38,40] observed that more than 85% of the total larval fish catch typically comprised mesopelagic fish larvae. As a result, these mesopelagic fish larvae proved to be reliable markers indicating the influx of the KBC into the Taiwan Strait. We propose that these species are carried into the waters of Taiwan Bank by the KBC. This conclusion finds support in the greater species number and abundance of myctophid larvae observed in spring (Table 2), indicating the accumulation of these taxa during this specific period. Similarly, Lee et al. [41] and Hsieh et al. [42,43] suggested that the intrusion of the KBC could potentially carry myctophid larvae from the Kuroshio region to the Taiwan Strait and the coastal waters off southwestern Taiwan, as supported by their respective studies. However, the concurrent existence of mesopelagic fish larvae in conjunction with larvae from epipelagic and demersal species, such as anchovies and gobiid fishes, likely suggests the potential for interspecific competition among these different species. This phenomenon arises due to the identification of mesopelagic fish larvae as potential competitors for the prey of economically significant fish larvae in oceanic regions, as indicated by studies such as Ahlstrom [44] and Sabatés and Masó [45].
Upwelling areas are often regarded as good fishing grounds because of the elevated primary productivity linked to the nutrients brought up by the upwelling process [14,15]. The rising bottom water in this study area provides an additional influx of nutrient-rich water, which, in turn, enhances the nutrients and phytoplankton, leading to an increase in the abundance of zooplankton [46,47,48]. In the present study, outstandingly high fluorescence values, indicating high phytoplankton biomass, were observed at stations situated within or near the upwelling area. Furthermore, our findings indicated a strong correlation between the distribution pattern of zooplankton abundance and fluorescence (Figure 4). In marine pelagic ecosystems, the population growth of zooplankton is typically associated with high phytoplankton biomass [47,48]. Without inputs from river discharges, we theorized that the heightened fluorescence and increased zooplankton abundance observed at the mentioned stations could be attributed to the upwelling of nutrients to the surface through topographic processes. Furthermore, during winter and early spring, the northeastern monsoon disrupts the thermal stratification during the summer, facilitating the transport of additional nutrients into the mixed layer through upwelling. This inference could be substantiated by the observation that fluorescence and zooplankton abundance in spring were slightly higher than in autumn throughout the study period. Similarly, elevated chlorophyll a concentration was documented in the Taiwan Bank Upwelling, as reported by studies conducted by Huang et al. [49] and Hsiao et al. [14].
Past studies have confirmed the crucial role of food availability in shaping the distribution and survival of fish larvae, particularly during the initial life stages, when the yolk is depleted [2,5]. Plankton aggregation and production enhancement in the upwelling area could provide favorable feeding conditions for fish larvae. However, physical factors such as seawater temperature and salinity also play a significant role in determining the survival of fish larvae in the initial phases of their life and influencing population recruitment success [2,5,50]. In this study, the findings from the distance-based linear model showed a clear distributional pattern of larval fish assemblage associated with seawater temperature and salinity (Table 5, Figure 7). During spring, specific mesopelagic fish larvae, including Diaphus slender type, Ceratoscopelus warmingii, and Myctophum asperum, were primarily observed on the southern side of the bank (such as at stations B7 and B17), where salinity levels were relatively higher. In contrast, these taxa were not present on the northern side of the bank (for example, stations B5, B10, and B14). Additionally, the distribution pattern of spring fish larvae exhibited a positive correlation with salinity. Taking into account the habitat of adult mesopelagic fishes, their larvae in the North Pacific are typically found in waters with high salinity levels [40,51]. We speculated that while the movements of the KBC or the SCSC bring mesopelagic fish larvae into the waters surrounding Taiwan Bank, the relatively lower salinity waters on the northern side of the bank during spring might not be suitable for mesopelagic fish larvae. This unfavorable environment could potentially lead to low larval survival despite the abundant food availability in this area.
Surface convergence resulting from upwelling can lead to the accumulation of diverse larval fish assemblages [4,52]. In the present study, the identification of the various families and their association with particular seasons contribute valuable insights into the ecological dynamics and life cycles of the observed fish species. Additionally, the diverse collection of fish larvae further emphasizes that the waters surrounding Taiwan Bank are recognized as a key transition zone between tropical and subtropical faunas [42,43]. This implies that the area plays a crucial role as a boundary where distinct ecological communities from both tropical and subtropical regions coexist or overlap. The diversity of fish larvae highlights the ecological richness and complexity of this transitional zone, emphasizing its importance in supporting a wide range of marine species representative of both tropical and subtropical environments.

5. Conclusions

In conclusion, this study demonstrated that the temporal change in larval fish abundance in autumn and spring was not significant; however, the diversity of fish larvae was higher in spring compared with autumn. The spatiotemporal occurrence of larval fish assemblage was significantly affected by the dominant currents and local hydrographic characteristics. The emergence of intense fluorescence and increased zooplankton abundance due to topographic upwelling provides a favorable food source for the larvae of fish. Furthermore, the correlation observed between hydrographic variables (specifically seawater temperature and salinity) and larval fish assemblages suggests the possible use of these assemblages as tracers for surface circulation in the waters surrounding Taiwan Bank.

Author Contributions

Conceptualization, H.-Y.H. and M.-A.L.; methodology, H.-Y.H. and P.-J.M.; software, H.-Y.H. and W.-L.C.; formal analysis, W.-L.C.; investigation, H.-Y.H. and W.-L.C.; resources, H.-Y.H. and P.-J.M.; writing—original draft preparation, H.-Y.H.; writing—review and editing, H.-Y.H. and P.-J.M.; supervision, H.-Y.H.; project administration, H.-Y.H. and M.-A.L.; funding acquisition, H.-Y.H. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Science Council and the Ministry of Education of the Republic of China, with funding given to H.-Y. Hsieh (MOST 110-2611-M-259-001).

Institutional Review Board Statement

This article did not harm fish and did not require ethical approval.

Data Availability Statement

Data is contained within the article.

Acknowledgments

We extend our appreciation to the captain and crew of the R/V New Ocean Researcher 3 for their proficient support in gathering zooplankton samples and additional hydrographic data.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. On 2 August 1998, a SeaWiFS image revealed elevated chlorophyll concentrations in regions experiencing upwelling: Pingtan Upwelling (PTU), Meizhou–Xiaman Upwelling (MXU), Dongshan Upwelling (DSU), Taiwan Bank Upwelling (TBU), and Penhu Upwelling (PHU). Cited from Tang et al. [12].
Figure 1. On 2 August 1998, a SeaWiFS image revealed elevated chlorophyll concentrations in regions experiencing upwelling: Pingtan Upwelling (PTU), Meizhou–Xiaman Upwelling (MXU), Dongshan Upwelling (DSU), Taiwan Bank Upwelling (TBU), and Penhu Upwelling (PHU). Cited from Tang et al. [12].
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Figure 2. Sampling locations in the waters surrounding Taiwan Bank in October 2021 and March 2022.
Figure 2. Sampling locations in the waters surrounding Taiwan Bank in October 2021 and March 2022.
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Figure 3. Temperature vertical profiles (°C, represented by black lines) and salinity variations (depicted in gray scales) for transects II~IV in the waters surrounding Taiwan Bank in October 2021 and March 2022.
Figure 3. Temperature vertical profiles (°C, represented by black lines) and salinity variations (depicted in gray scales) for transects II~IV in the waters surrounding Taiwan Bank in October 2021 and March 2022.
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Figure 4. Zooplankton abundance (ind. m−3) in the waters surrounding Taiwan Bank in (A) October 2021 and (B) March 2022.
Figure 4. Zooplankton abundance (ind. m−3) in the waters surrounding Taiwan Bank in (A) October 2021 and (B) March 2022.
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Figure 5. Abundance of fish larvae (ind. 1000 m−3) in the waters surrounding Taiwan Bank in (A) October 2021 and (B) March 2022.
Figure 5. Abundance of fish larvae (ind. 1000 m−3) in the waters surrounding Taiwan Bank in (A) October 2021 and (B) March 2022.
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Figure 6. Cluster dendrogram and two-dimensional MDS ordination of Bray–Curtis similarity, based on a matrix of log (x + 1)-transformed abundance data for the 18 predominant taxa with abundance greater than 1%. Abbreviations are as follows: O = October; M = March.
Figure 6. Cluster dendrogram and two-dimensional MDS ordination of Bray–Curtis similarity, based on a matrix of log (x + 1)-transformed abundance data for the 18 predominant taxa with abundance greater than 1%. Abbreviations are as follows: O = October; M = March.
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Figure 7. Distance-based redundancy analysis (dbRDA) biplot for environmental variables and larval fish assemblages.
Figure 7. Distance-based redundancy analysis (dbRDA) biplot for environmental variables and larval fish assemblages.
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Table 1. Mean (±SD) of four environmental variables (at 10 m), zooplankton abundance, total abundance, species number, Shannon diversity (H’), and Pielou evenness (J’) of fish larvae in the waters surrounding Taiwan Bank in October 2021 and March 2022.
Table 1. Mean (±SD) of four environmental variables (at 10 m), zooplankton abundance, total abundance, species number, Shannon diversity (H’), and Pielou evenness (J’) of fish larvae in the waters surrounding Taiwan Bank in October 2021 and March 2022.
VariableOctober 2021March 2022
Environmental variables
Temperature (°C)27.87 ± 0.6723.11 ± 1.70
Salinity33.95 ± 0.1234.15 ± 0.15
Fluorescence (mg m−3)0.66 ± 0.510.72 ± 0.53
Zooplankton (ind. m−3)381 ± 227451 ± 226
Fish larvae
Abundance (ind. 1000 m−3)480 ± 363362 ± 364
Species number (total)14 ± 6 (66)18 ± 2 (105)
Species diversity (H’)1.96 ± 0.521.99 ± 0.77
Species evenness (J’)0.75 ± 0.140.76 ± 0.13
Table 2. The most frequent captured families (>1% of the total fish larvae) in the waters surrounding Taiwan Bank in October 2021 and March 2022.
Table 2. The most frequent captured families (>1% of the total fish larvae) in the waters surrounding Taiwan Bank in October 2021 and March 2022.
FamilyOctober 2021FamilyMarch 2022
Number of TaxaContribution of Family to Total Abundance (%)Number of TaxaContribution of Family to Total Abundance (%)
Engraulidae226.23Myctophidae1436.84
Gobiidae516.45Clupeidae112.90
Apogonidae114.07Ammodytidae16.88
Bregmacerotidae29.50Gobiidae23.39
Myctophidae108.55Sparidae53.36
Trichiuridae13.38Trichiuridae23.09
Percichthyidae33.16Mullidae22.84
Bothidae31.49Scombridae62.69
Sciaenidae21.29Nomeidae22.45
Trichonotidae11.17Mugilidae12.21
Labridae31.13Tetraodontidae22.09
Synodontidae31.17
Gempylidae31.11
Pleuronectidae21.10
Carangidae101.01
Total3386.41Total5683.13
Table 3. Mean abundance (ind. 1000 m−3) and relative abundance (RA, %) of the dominant fish larvae (>1% of the total fish larvae) in the waters surrounding Taiwan in October 2021 and March 2022.
Table 3. Mean abundance (ind. 1000 m−3) and relative abundance (RA, %) of the dominant fish larvae (>1% of the total fish larvae) in the waters surrounding Taiwan in October 2021 and March 2022.
TaxonOctober 2021TaxonMarch 2022
Mean ± SDRAMean ± SDRA
Engraulis japonicus117 ± 30724.38Diaphus slender type67 ± 16618.38
Apogon sp.63 ± 9713.14Clupeidae gen. sp.47 ± 13912.90
Gobiidae gen. spp.56 ± 6811.59Benthosema pterotum38 ± 5310.42
Bregmaceros sp.31 ± 616.41Bleekeria mitsukurii25 ± 426.88
Myctophidae gen. spp.17 ± 153.59Gobiidae gen. spp.12 ± 283.31
Tridentiger sp.16 ± 263.38Trichiurus lepturus10 ± 142.86
Trichiurus lepturus15 ± 263.15Cubiceps pauciradiatus9 ± 92.39
Bregmaceros nectabanus12 ± 202.47Planiliza sp.8 ± 172.21
Notoscopelus resplendens11 ± 322.32Mullidae gen. sp.8 ± 202.09
Lateolabrax sp.7 ± 181.40Takifugu sp.8 ± 162.09
Percichthyidae gen. sp.7 ± 111.40Diaphus stubby type7 ± 161.83
Asterorhombus sp.5 ± 141.09Sparidae gen. spp.6 ± 101.69
Nibea sp.5 ± 151.09Ceratoscopelus warmingii6 ± 131.68
Acanthopagrus sp.6 ± 171.52
Myctophum sp.5 ± 101.34
Scomberomorus spp.4 ± 121.07
Table 4. Discriminating larval fish taxa of three station groups with the analysis of the abundance of the top 18 dominant taxa using SIMPER, with a cutoff set to 90% for low contributions. Sim/SD: the ratio between the taxon contribution to within-group similarity and the standard deviation; C: percentage contribution to within-group average similarity.
Table 4. Discriminating larval fish taxa of three station groups with the analysis of the abundance of the top 18 dominant taxa using SIMPER, with a cutoff set to 90% for low contributions. Sim/SD: the ratio between the taxon contribution to within-group similarity and the standard deviation; C: percentage contribution to within-group average similarity.
Average Similarity (%)A (–) B (43.21) C (30.51)
Sim/SDC (%) Sim/SDC (%) Sim/SDC (%)
Less than two samples
in group		 Gobiidae gen. spp.3.8835.54Benthosema pterotum1.4936.77
Myctophidae gen. spp.1.3324.89Cubiceps pauciradiatus0.6633.39
Apogon sp.0.6412.52Trichiurus lepturus0.5711.14
Engraulis japonicus0.506.46Bleekeria mitsukurii0.367.54
Trichiurus lepturus0.456.33Planiliza sp.0.292.91
Tridentiger sp.0.495.13
Total-90.87Total-91.75
Table 5. Percentages of variation in larval fish assemblage explained by individual environmental explanatory variables, incorporated into the distance-based linear models for sampling stations. Asterisks denote environmental variables that significantly explain a percentage of the variation in larval fish assemblage; SS: sum of squares.
Table 5. Percentages of variation in larval fish assemblage explained by individual environmental explanatory variables, incorporated into the distance-based linear models for sampling stations. Asterisks denote environmental variables that significantly explain a percentage of the variation in larval fish assemblage; SS: sum of squares.
VariableSS (Trace)Pseudo-Fp-Value% Variation Explained
Temperature150215.84730.001 *26.76
Salinity7355.12.41300.026 *13.10
Bottom depth2663.60.79710.6114.74
Fluorescence2915.70.87670.5155.19
Zooplankton2679.50.80210.5854.77
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Hsieh, H.-Y.; Lee, M.-A.; Chiu, W.-L.; Meng, P.-J. Comparison of Abundance and Structure of Larval Fish Assemblages between Autumn and Spring in the Waters Surrounding Taiwan Bank, Western North Pacific. Fishes 2024, 9, 16. https://doi.org/10.3390/fishes9010016

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Hsieh H-Y, Lee M-A, Chiu W-L, Meng P-J. Comparison of Abundance and Structure of Larval Fish Assemblages between Autumn and Spring in the Waters Surrounding Taiwan Bank, Western North Pacific. Fishes. 2024; 9(1):16. https://doi.org/10.3390/fishes9010016

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Hsieh, Hung-Yen, Ming-An Lee, Wei-Lun Chiu, and Pei-Jie Meng. 2024. "Comparison of Abundance and Structure of Larval Fish Assemblages between Autumn and Spring in the Waters Surrounding Taiwan Bank, Western North Pacific" Fishes 9, no. 1: 16. https://doi.org/10.3390/fishes9010016

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