Eco-Dynamic Analysis of the Community Structure of Nekton in the Northern South China Sea

Abstract

The universal laws of thermodynamics in the process of ecosystem development have long been the common research focus of ecology and biophysics. Eco-exergy from thermodynamics is a popular theory in the study of ecosystem self-organization that has been widely used in the study of wetlands and aquatic ecosystems. This study is based on the data of bottom trawl fishery resources in the Northern South China Sea in 1964–1965, 1997–1999, 2006–2007, and 2017. Based on the eco-exergy theory, the exergy contribution rate (P_C) of the nekton community and the exergy contribution rate (P_L) of different organismic populations were constructed. The eco-exergy (E_X) and specific eco-exergy (E_Xsp) of the nekton in the northeastern South China Sea were analyzed. The results show that, from 1964 to 2017, the E_X and E_Xsp of the nekton community decreased 13.28-fold and 1.42-fold, respectively. Fish populations remained the major contributors to the E_X and E_Xsp of the nekton community; however, compared to crustaceans and cephalopods, their role in maintaining the stability and complexity of the community structure was gradually weakened, and the genetic information per unit of biomass decreased. Meanwhile, compared to fish, the proportion of the E_X of crustaceans and cephalopods in the nekton community showed an upward trend. The proportion of crustaceans increased from 2.76% in 1997–1999 to 14.84% in 2017, while that of cephalopods increased from 3.55% to 16.67%. Based on the findings, we speculate that crustaceans and cephalopods play an increasing role in the stability and complexity of the fishery resource structure in the Northern South China Sea. The species replacement in the nekton was obvious, and the dominant species of the Nekton community gradually changed from k-type species to r-type species in the Northern South China Sea.

1. Introduction

Energy is the driving force of ecosystem processes, and all life activities in the system are accompanied by energy transformation and transmission [1]. Therefore, the universal laws of thermodynamics in the process of ecosystem development have long been the common research focus of ecology and biophysics [2]. Eco-exergy is a research method applying thermodynamic concepts to the field of ecology. It is a measure of the maximum amount of work an ecosystem can do to reach thermodynamic equilibrium with its environment, indicating the distance between the ecosystem’s current state and its equilibrium with the surrounding abiotic environment [3]. It expresses the function of an ecosystem through the conversion of matter and energy in the process of ecosystem metabolism, that is, it explains the changes in the internal attributes of an ecosystem through the biomass and the genetic information contained therein. The eco-exergy theory method realizes the unified measurement of the inorganic environment and biological community structure [4]. This means that during ecological succession, eco-exergy is used to accumulate biomass, which in turn stores eco-exergy [5]. Thus, eco-exergy represents a measure of structural biomass and information about embedded biomass.

Eco-exergy is often used as an evaluation index to evaluate the health status and development level of marine ecosystems [6]. As a holistic indicator, eco-exergy expresses the development degree of an ecosystem, which means how developed an ecosystem was and how difficult it would be to destroy it [7]. Fishery resources are an important part of marine ecosystems, and the change in marine ecosystems will affect the structure of fishery resources. Eco-exergy was used as an index to evaluate the changes in the community structure of fishery resources, which could reflect the changes in fishery resource biomass and embedded biomass information [8,9]. With the increasing understanding of marine ecology and the increasing attention paid to the impacts of human activities such as fisheries, the concept of ecosystem-based fisheries management (EBFM) has been accepted by more and more researchers and international organizations in order to maintain the health of fisheries ecosystems and achieve sustainable ecosystem services [10].

The world fisheries statistics released by FAO show this in the context of the continuous increase in global fishing efforts. The total production of capture fisheries has been gradually flat or slightly decreased since the 1990s, and the proportion of fully and overexploited resources has gradually increased. The overall CPUE has decreased significantly [11]. Many studies have reported the collapse of fisheries resources worldwide [12,13,14,15]. Due to the interference of human activities such as overfishing and industrial construction, the habitats of offshore fishery resources in the South China Sea have been destroyed, fishery resources have declined, and the community structure has been altered [16,17,18]. The phenomenon of the young age, miniaturization, and low quality of caught fish due to habitat destruction and resource decline has become a representative feature of the fishery resources in the offshore waters of the South China Sea [19,20,21,22]. The South China Sea is a semi-closed sea area. It is also the area with the most rapid development of industrialization and urbanization, and its fishery resources are highly developed [23]. The northern coastal waters of the South China Sea are important areas for traditional fishery production in China. How to restore the damaged fishery resources and habitats and improve the health of the marine ecosystem have always been hot issues in the conservation of marine fishery resources [24,25,26]. Studies have shown that artificial reef construction, fishery enhancement, and marine ranching construction can accelerate the restoration of regionally degraded fishery resources and habitats [27,28]. The marine ecosystem is a typical self-organizing system with self-repair ability [29], and its structure and function show a complex nonlinear development law [30]. At present, most studies on the community structure of the fishery resources in the northern South China Sea have only involved local sea areas or a certain season, and the taxonomic biodiversity has been used to illustrate the community of fishery resources in the northern coastal waters of the South China Sea [31,32,33,34]. There have been few reports analyzing the community structure of the fishery resources in the northern South China Sea from an eco-exergy perspective, and studies on the long-term changes in the community structure of fishery resources in the northern South China Sea from an eco-exergy perspective are particularly lacking. The development dynamics of the community structure of fishery resources based on eco-exergy remain to be revealed.

The purpose of this study is to analyze the changes in the nekton community structure in the northern South China Sea from the perspective of ecological exergy. The eco-exergy evaluation index was used to analyze the community structure of the nekton from 1964 to 2017, and the community structure of the nekton during these 53 years was compared in an attempt to answer the following two questions: (1) How did the Eco-Exergy (E_X) and Specific Eco-Exergy (E_Xsp) of the nekton community change? (2) What are the changing characteristics of the exergy contribution rates of the Community (P_C) and the Population (P_L) in fish, crustacean, and cephalopod populations? By answering these two questions, we could determine the dynamic characteristics of the nekton community in the northern South China Sea. The research methods used in this study can provide a new evaluation method for marine fishery resource conservation and ecological restoration effect evaluation, and the results can provide support for the formulation and implementation of fishery resource development and management in the South China Sea.

2. Materials and Methods

2.1. Fishery Data

The data used in this assessment were derived from surveys of fishery resources obtained through bottom trawling in the Northeastern South China Sea in 1964–1965, 1997–1999, 2006–2007, and 2017. The surveys were conducted in accordance with the requirements of the Specifications for Oceanographic Survey; the trawling time of each station was 1 h, the average towing speed was 3 knots, and the trawl nets were set 2–3 nautical miles away from the set stations.

In 1964–1965, 1997–1999, 2006–2007, and 2017, 55 stations, 87 stations, 46 stations, and 45 stations were set up, respectively, in the coastal waters of the northern part of the South China Sea, and the survey stations in each year were arranged in a checkerboard pattern. The three surveys (1964–1965, 1997–1999, and 2006–2007) were conducted in spring, summer, autumn, and winter each time. The 2017 survey was conducted in spring and autumn. In each survey, one bottom trawl was conducted at each station. The nekton data used in this study are the average values of each season, that is, the nekton data in 1964–1965 are the average values of the spring, summer, autumn, and winter of 1964–1965, and the nekton data in 1997–1999 and 2006–2007 are also the average values of the spring, summer, autumn, and winter. The 2017 nekton data is the seasonal average of spring and summer in 2017.

The survey vessels used in the four surveys were all bottom trawlers, and the nets used were nylon bottom trawlers. The net parameters are shown in

Table 1. Parameters of the nets in surveys.

Survey Time	Net Width (m)	Net Length (m)	Net Port Mesh Size (cm)	Cod End Mesh Size (cm)
1964–1965	10.7	29	6.4	2.5
1997–1999	18	78.2	20	2.4
2006–2007	24.4	60.6	10	4
2017	16	32	10	5

.

2.2. Study Area

The survey of the fishery resources in the northern South China Sea covered the shallow waters below the 200 m isobath in the northern South China Sea (Figure 1). The water depth in the study area gradually deepened from north to south and southeast. The coastal waters of 0–100 m in the study area are mainly affected by the coastal current, and the coastal waters of 100–200 m are mainly affected by the South China Sea warm current [35]. The surface sediments in the northern South China Sea are composed of terrigenous clasts, biogenic groups, authigenic minerals, volcanic clasts, and meteorite particles, which are mainly in the form of sand, silt, and clay, and the gravel content is relatively low [36,37,38]. The percentage of coarse particles in the waters near the intersection of the continental shelf and continental slope is higher than that on both sides, while the content of fine particles in the deep sea is higher [39].

2.3. Data Analysis

2.3.1. Biomass of the Nekton (D)

This index reflects the current total status of fishery resources. The calculation formula is as follows:

$$D=\frac{C}{qa},$$

where C is the average trawl net catch per hour (kg/h), q is the net capture rate (0.5 for the nekton) [40], and a is the sampling area (km²). Since the data distribution trend did not conform to the normal distribution, the Mann-Whitney U test was used for significance difference analysis.

2.3.2. E_X and E_Xsp

In the late 1970s, eco-exergy theories and methods were introduced into ecological research. At present, some research fields, such as grassland, and forest ecosystems, have relatively complete calculations and theoretical systems to evaluate changes in community structure. Ex considers the chemical energy stored in biomass and the information embodied in genes which could be used to indicate the state of ecosystem health and level of development [41]. Ex_sp expresses the ability of an ecosystem to utilize the available resources [42]. Ex and Ex_sp are calculated according to the following formulas:

$$Ex=18.7\left(\frac{\mathrm{K}\mathrm{J}}{\mathrm{g}}\right)\sum _{i=0}^n{C}_i{\beta }_i,$$

$${Ex}_{sp}=\frac{\left[18.7\left(\frac{\mathrm{K}\mathrm{J}}{\mathrm{g}}\right)\sum _{i=0}^n{C}_i{\beta }_i\right]}{\sum _{i=0}^n{C}_i},$$

where 18.7 kJ/g is the mean eco-exergy of organic matter and detritus, C_i is the biomass of the ith species (g/m²), and β_i is the weighting factor of the ith species relative to detritus [43]. β_i is calculated using the following formula:

$$\beta =1+\left[\frac{\ln \left({20}^{1.65\times {10}^{8}c}\right)}{7.43\times {10}^5}\right],$$

where the C value represents the total physical length of biological haploid genomic DNA in pg or 10⁻¹² g, which was derived in this study from the Animal Genome Size Database (http://www.genomesize.com/index.php, accessed on 23 April 2023) [44]. Quoting should be as precise as possible at the species level [45]. If the species could be determined, the corresponding C values of each species were used; if the species could not be determined, the C value of a species from the same genus was used for the calculation.

2.3.3. P_C and P_L

The two indices reflect the contribution of a species to its community and population respectively [46]. The calculation formulas are as follows:

$$P_C=\frac{\sum _{i=1}^n{Ex}_{ij}}{\sum _{i=1}^n\sum _{j=1}^{mi}{Ex}_{ij}}\times 100\%,$$

$$P_L=\frac{{Ex}_{ij}}{\sum _{j=1}^{mi}{Ex}_{ij}}\times 100\%,$$

where mi is the number of species contained in fishery resource population i, n is the number of fishery resources contained in the community, and Ex_ij is the eco-exergy of species j of population i of fishery resources. Since the data distribution trend did not conform to the normal distribution, the Mann-Whitney U test was used for significance difference analysis.

2.3.4. The Trophic Level of Fish

This index reflects the nutrient structure characteristics of the fish community [47]. Trophic level data of fish adopted from FishBase (www.fishbase.se/search.php, accessed on 23 April 2023). The calculation formulas are as follows:

$$TL=\frac{\sum _{i=1}^m{TL}_i\times y_i}{Y}$$

where TL_i is the nutrient level of fish i, y_i is the biomass of fish i; Y is the total biomass of the fish population.

3. Results

3.1. Fishery Resource Biomass

The total mean biomass of the nekton in the northern South China Sea during 1964–1965 was 2156.30 kg/km². The total mean biomass of the nekton during 1997–1999, 2006–2007, and 2017 were 658.80 kg/km², 1084.39 kg/km², and 421.03 kg/km², respectively, showing an overall decreasing trend (Figure 2). According to the results of the Mann-Whitney U test, the biomass of the Nekton in 1964–1965 was significantly higher than that in 1997–1999, 2006–2007, and 2017 (p < 0.01), and the biomass of the Nekton in 2006–2007 was significantly higher than that in 2017 (p < 0.05), but there was no significant difference among other years (p > 0.05).

3.2. E_X and E_Xsp

In the 53 years from 1964 to 2017, the E_X and E_Xsp of the nekton in the fishery resources decreased 13.28-fold and 1.42-fold, respectively, and the community structure tended to be disordered and simplified. The E_X of the fish population accounted for 93.7%, 79.0%, and 68.5% of the nekton community in 1997–1999, 2005–2006, and 2017, respectively. These proportions showed a downward trend. However, the fish population remained the major contributor to the fishery resource community. Compared to the fish populations, the E_X values of the crustacean and cephalopod populations showed an upward trend. The proportion of crustaceans increased from 2.76% in 1997–1999 to 14.84% in 2017, while that of cephalopods increased from 3.55% to 16.67%. (Figure 3 and Figure 4).

3.2.1. Dynamics of Fish Population Structure

Overall, the E_X values of the fish populations showed an obvious downward trend (Figure 3). E_X decreased 18.39-fold from 48,887 kJ/m² to 2520.49 kJ/m² in the 53 years from 1964 to 2017. The E_X of the fish population structure decreased 10.23-fold in the 33 years from 1964 to 1997, increased 0.91-fold in the 10 years from 1997 to 2007, and then decreased again 2.30-fold in the 10 years from 2007 to 2017. The E_Xsp of the fish population showed a trend of continuous decline in the 53 years from 1964 to 2017 (Figure 4) from 12,370.90 kJ/g to 9231.04 kJ/g, reflecting a 0.34-fold decrease.

With reference to the value of fish trophic level in FishBase, we analyzed the trophic structure of fish populations in the four surveys. The results showed that in 1964–1965, 1997–1999, 2006–2007, and 2017, the average nutrient levels of fish in the northern South China Sea were 4.127, 4.060, 3.872, and 3.798, respectively, showing a decreasing trend.

3.2.2. Dynamics of Crustacean Population Structure

The E_X of the crustacean population showed a trend of first rising and then falling (Figure 3). Compared to the fish populations, the E_X of the crustacean population changed relatively gently. During the 20 years from 1997 to 2017, the E_X of the crustaceans increased 3.27-fold from 128.02 kJ/m² to 546.19 kJ/m². It increased 10.49-fold in the 10 years from 1997 to 2007 but decreased about 1.70-fold in the 10 years from 2007 to 2017. The E_Xsp of the crustacean population declined continuously from 9888.70 kJ/g to 7760.34 kJ/g during the 20 years from 1997 to 2017 (Figure 4), reflecting a 0.27-fold decrease. In the 10 years from 1997 to 2007, the E_Xsp of the crustacean population did not change significantly, decreasing only 0.02-fold, whereas in the 10 years from 2007 to 2017, it exhibited a significant 0.2-fold decrease.

3.2.3. Dynamics of Cephalopod Population Structure

The E_X of the cephalopod population generally showed an increasing trend (Figure 3). During the 20 years from 1997 to 2017, the E_X of the cephalopod population increased 2.72-fold from 165.02 kJ/m² to 613.41 kJ/m². It increased 3.52-fold in the 10 years from 1997 to 2007 but decreased about 0.80-fold in the 10 years from 2007 to 2017. During the 20 years from 1997 to 2017, the E_Xsp of the cephalopod population showed a continuously rising trend (Figure 4) from 4708.65 kJ/m² to 7908.68 kJ/m², reflecting a 1.68-fold increase. This value increased 0.68-fold in the 10 years from 1997 to 2007 and 0.36-fold in the 10 years from 2007 to 2017.

3.3. P_C and P_L

The species living in a community always occupy a certain resource space and affect the energy flow. This thermodynamic effect can be measured using P_C and P_L. P_C and P_L of species are time functions. Analyzing the changes in P_C and P_L on a timescale can be used to understand the growth of a species in a community from the perspective of thermodynamics.

3.3.1. Changes in the Statuses of Species in the Nekton Community

As can be seen in

Table 2. The P_C values of the main species of the Nekton in the Northern South China Sea.

Species	PC (%)
	1964–1965	1997–1999	2006–2007	2017
Carcharhinus amblyrhynchos Bleeker, 1856	13.100	—	—	—
Navodon septentrionalis (Günther, 1874)	5.592	0.057	0.001	—
Nemipteras bathybius Snyder,1911	4.568	1.132	3.465	2.280
Lutjanus erythopterus (Cuvier, 1828)	4.066	0.137	—	0.013
Dasyatis zugei (Müller & Henle, 1841)	3.723	0.101	—	0.014
Pristipomoides typus Bleeker, 1852	3.446	0.101	0.062	—
Saurida tumbil (Bloch, 1795)	3.112	9.986	1.283	2.086
Upeneus moluccensis (Bleeker, 1855)	2.621	0.072	—	—
Argyrosomus microcephalus (Tang, 1937)	2.063	0.217	0.026	0.149
Saurida filamentosa Ogilby, 1910	1.929	0.683	0.571	0.704
Pampus cinereus (Bloch, 1795)	1.742	0.268	0.338	0.002
Muraenesox cinereus (Forsskål, 1775)	1.742	0.862	1.117	2.541
Pomadasys hasta (Bloch, 1790)	1.610	0.104	—	—
Gymnocranius griseus (Temminck & Schlegel, 1843)	1.483	0.102	—	—
Saurida undosquamis (Richardson, 1848)	1.432	8.418	1.002	2.068
Priacanthus macracanthus Cuvier, 1829	1.235	1.677	0.352	0.070
Nemipteras virgatus (Houttuyn, 1782)	1.012	2.873	0.613	1.821
Parargyrops edita Tanaka, 1916	0.958	1.877	1.026	0.395
Trichiurus haumela (Forsskål, 1775)	0.910	3.852	1.053	1.120
Polynemus sextarius Bloch & Schneider, 1801	0.595	0.027	2.363	2.701
Upeneus bensasi (Temminck & Schlegel, 1843)	0.451	0.237	1.790	0.600
Siganus oramin (Bloch & Schneider, 1801)	—	2.955	0.219	4.043
Thamnaconus hypargyreus (Cope, 1871)	—	2.499	2.387	0.449
Trachinocephalus myops (Forster, 1801)	—	0.108	1.486	2.217
Trichiurus brevis Wang & You, 1992	—	3.908	0.219	—
Raja hollandi Jordan & Richardson, 1909	—	2.093	0.222	0.750
Champsodon capensis Regan, 1908	—	2.010	0.986	0.347
Apogon semilineatus Temminck & Schlegel, 1842	—	1.957	0.269	0.226
Synodus kaianus (Günther, 1880)	—	1.580	0.540	—
Trachurus japonicus (Temminck & Schlegel, 1844)	—	0.122	2.461	0.859
Malakichthys griseus Döderlein, 1883	—	0.004	2.039	—
Lophiomus setigerus (Vahl, 1797)	—	0.343	1.399	0.822
Arnoglossus tenuis Günther, 1880	—	0.063	0.037	5.491
Penaeus monodon Fabricius, 1798	—	0.004	0.130	0.186
Penaeus japonicus Spence Bate, 1888	—	0.009	0.003	0.114
Penaeus penicillatus Alcock, 1905	—	0.001	0.006	0.084
Ibacus novemdentatus Gibbes, 1850	—	0.029	0.057	0.001
Solenocera crassicornis (H. Milne Edwards, 1837)	—	0.025	3.751	1.900
Portunus sanguinolentus (Herbst, 1783)	—	0.043	3.602	0.906
Portunus trituberculatus (Miers, 1876)	—	0.011	0.131	0.143
Portunus gracilimanus (Stimpson, 1858)	—	0.001	0.006	0.866
Portunus argentatus (Alcock, 1899)	—	0.419	0.121	0.459
Portunus haanii (Stimpson, 1858)	—	0.072	0.294	0.273
Portunus pelagicus (Linnaeus, 1758)	—	0.001	0.008	0.015
Calappa philargius (Linnaeus, 1758)	—	0.018	0.334	0.472
Charybdis feriatus (Linnaeus, 1758)	—	0.176	2.188	0.433
Charybdis miles (De Haan, 1835)	—	0.849	0.197	1.843
Oratosquilla nepa (Serville & Guérin, 1828)	—	0.001	0.146	0.039
Harpiosquilla raphidea (Fabricius, 1798)	—	0.010	0.017	0.006
Oratosquilla oratoria (De Haan, 1844)	—	0.001	0.414	0.223
Oratosquilla inornata (Tate, 1883)	—	0.004	0.002	0.019
Loligo edulis Hoyle, 1885	—	1.551	1.261	2.930
Loligo duvaucelii Loligo Lamarck, 1798	—	0.152	0.860	3.443
Loligo chinensis Gray, 1849	—	0.047	1.474	1.777
Loligo tagoi Sasaki, 1929	—	0.024	0.047	2.659
Sepioteuthis lessoniana Sepioteuthis Blainville, 1824	—	0.022	0.129	0.039
Sepia esculenta Hoyle, 1885	—	0.158	0.388	0.807
Euprymna berryi Sasaki, 1929	—	0.011	0.015	0.121
Sepia pharaonic Ehrenberg, 1831	—	0.170	0.392	0.004
Sepia lycidas Gray, 1849	—	0.041	0.234	0.017
Octopus variabilis (Sasaki, 1929)	—	0.025	0.179	0.187
Octopus ocellatus Gray, 1849	—	0.001	0.171	0.603
Octopus variabilis (Sasaki, 1929)	—	0.004	0.049	2.792
Other species	42.611	45.694	56.064	44.869
Total	100	100	100	100

Note: “—” indicates that no data were recorded in the trawling survey.

, in the trawl survey in 1964–1965, the P_C of Carcharhinus menisorrah was the largest at 13.100%, but this species did not appear in the three subsequent surveys. The total P_C of the 22 species in the trawl survey in 1964–1965 was 57.389%. In the 1997–1999 trawl surveys, the P_C of Saurida tumbil was the largest at 9.986%. The total P_C of the 62 species in the trawl survey in 1997–1999 was 54.306%. In the trawl survey of 2006–2007, the P_C of Solenocera crassicornis was the largest at 3.751%, and 48 species accounted for 43.936% of the total. In the trawl survey of 2017, the P_C of Arnoglossus tenuis was the largest at 5.491%, and a total of 54 species accounted for 55.131% of the catches. The results showed that the 63 species listed in Table 2 were the main species of the nekton community in the northern South China Sea for a long time, and these species played a major role in maintaining the stability of the nekton community structure.

In terms of the annual P_C trends of the main species, among the 33 species of fish, only five species showed increasing trends: Muraenesox cinereus, Polynemus sextarius, Siganus oramin, Trachinocephalus myops, and Arnoglossus tenuis, while the other 28 species showed decreasing trends. The P_C values of large economic species, such as Carcharhinus menisorrah, Lutjanus erythopterus, Dasyatis zugei, Pristipomoides typus, Upeneus moluccensis, Pampus nozawae, and Parargyrops edita, decreased significantly. The P_C and P_L values of crustaceans and cephalopods in the South China Sea fishery resource communities increased year by year, with 16 of 18 crustaceans and 10 of 12 cephalopods showing increasing trends (Table 2).

3.3.2. Changes in the Statuses of Species in the Fish Population

In the fish population, the highest P_L values in 1964–1965, 1997–1999, 2006–2007, and 2017 were Carcharhinus menisorrah, Saurida tumbil, Saurida undosquamis, and Arnoglossus tenuis, with P_L values of 13.100%, 10.658%, 8.985%, and 8.017%, respectively. The maximum contribution rate in each year when the fishery was performed showed a gradually decreasing trend, indicating that the dominant species status in the fish population gradually weakened. The total P_L values of the 43 fish species listed in

Table 3. The P_L values of the main species of the fish population in the Northern South China Sea.

Species	PL (%)
	1964–1965	1997–1999	2006–2007	2017
Carcharhinus menisorrah Bleeker, 1856	13.100	—	—	—
Saurida tumbil (Bloch, 1795)	3.112	10.658	1.625	3.046
Saurida undosquamis (Richardson, 1848)	1.432	8.985	1.269	3.019
Arnoglossus tenuis Günther, 1880	—	0.067	0.046	8.017
Siganus oramin (Bloch & Schneider, 1801)	—	3.154	0.278	5.903
Navodon septentrionalis (Günther, 1874)	5.592	0.0002	0.001	—
Nemipteras bathybius Snyder,1911	4.568	1.208	4.389	3.329
Trichiurus brevis Wang & You, 1992	—	4.171	0.278	—
Trichiuru haumela (Forsskål, 1775)	0.910	4.111	1.334	1.635
Lutjanus erythopterus (Cuvier, 1828)	4.066	0.307	—	0.020
Polynemus sextarius Bloch & Schneider, 1801	0.595	0.028	2.993	3.944
Acropoma japonicum Günther, 1859	—	3.780	0.540	1.609
Dasyatis zugei (Müller & Henle, 1841)	3.723	0.115	—	0.021
Muraenesox cinereus (Forsskål, 1775)	1.742	0.920	1.415	3.710
Dactyloptena peterseni (Nystrom, 1908)	—	0.065	3.599	—
Leiognathus bindus Valenciennes, 1835	0.904	3.535	0.250	0.011
Pristipomoides typus Bleeker, 1852	3.446	0.042	0.079	—
Trachinocephalus myops (Forster, 1801)	—	0.751	1.882	3.238
Trachurus japonicus (Temminck & Schlegel, 1844)	—	1.062	3.117	1.254
Nemipteras virgatus (Houttuyn, 1782)	1.012	3.066	0.776	2.658
Navodon xanthopterus (Cope, 1871)	—	2.667	3.023	0.656
Urolophus marmoratus Chu, Hu & Li, 1981	—	—	2.990	—
Upeneus moluccensis (Bleeker, 1855)	2.621	0.047	—	—
Malakichthys griseus Döderlein, 1883	—	0.005	2.583	—
Crossorhombus azureus (Alcock, 1889)	—	0.001	0.004	2.478
Upeneus japonicus Houttuyn, 1782	—	—	—	2.447
Upeneus bensasi (Temminck & Schlegel, 1843)	0.451	0.253	2.267	0.877
Raja hollandi Jordan & Richardson, 1909	—	2.234	0.281	1.095
Sparus latus (Houttuyn, 1782)	—	0.107	0.475	2.216
Champsodon capensis Regan, 1908	—	2.146	1.249	0.506
Apogon semilineatus Temminck & Schlegel, 1842	—	2.088	0.340	0.329
Argyrosomus microcephalus (Tang, 1937)	2.063	0.232	0.033	0.217
Parargyrops edita Tanaka, 1916	0.958	2.003	1.300	0.576
Acropoma hanedai (Matsubara, 1953)	—	0.0001	1.799	—
Priacanthus macracanthus Cuvier, 1829	1.235	1.790	0.446	0.103
Lophiomus setigerus (Vahl, 1797)	0.609	0.366	1.772	1.200
Pampus cinereus (Bloch, 1795)	1.742	0.019	0.429	0.003
Synodus kaianus (Günther, 1880)	—	1.687	0.684	—
Raja kenojei (Müller et Henle,1841)	—	0.070	1.626	—
Pomadasys hasta (Bloch, 1790)	1.610	0.007	—	—
Harpodon nehereus Hamilton, 1822	—	0.005	1.518	0.355
Gymnocranius griseus (Temminck & Schlegel, 1843)	1.483	0.020	—	—
Saurida elongate (Temminck & Schlegel, 1846)	—	0.729	0.724	1.028
Other species	43.028	37.497	52.586	44.502
Total	100	100	100	100

Note: “—” indicates that no data were recorded in the trawling survey.

accounted for 56.972%, 62.503, 47.414%, and 55.498% of the total P_L of the fish population in 1964–1965, 1997–1999, 2006–2007, and 2017, respectively. Since P_L reflects the contribution of species to the stability of population structure and the contributions of these 43 species to the whole fish population were more than 50% in each survey, thus, we speculate that these 43 species were the main ones maintaining the stability of the fish population structure in the Northern South China Sea over a large timescale (53 years).

Among the 43 species of fish, the P_L values of Saurida tumbil, Saurida undosquamis, and Nemipteras bathybius were all greater than 1.2% in each year and were generally higher than those of most other species in each year, indicating that these three species were the dominant species in the northern South China Sea. According to the survey data, Carcharhinus menisorrah, with the largest P_L of 13.100% in 1964–1965, did not appear in the surveys of 1997–1999, 2006–2007, and 2017. The P_L values of dominant species, such as Navodon septentrionalis, Lutjanus erythopterus, Dasyatis zugei, and Pristipomoides typus, decreased significantly in 1997–1999, 2006–2007, and 2017, indicating that these species gradually lost their important roles in the population structure. The total P_L values of the dominant species decreased from 21.511% to 0.697%, indicating that, over a large timescale (53 years), these species gradually lost their dominant status in the fish population. Small and medium-sized fish such as Arnoglossus tenuis, Siganus oramin, Polynemus sextarius, Trachinocephalus myops, Crossorhombus azureus, Sparus latus, and Saurida elongata gradually became the new dominant species of the fish population. The total P_L of these species increased from 0.595% to 30.767%. According to the results of the Mann-Whitney U test, P_L values of the main species of the fish population were significantly higher in 1964–1965 than in 1997–1999, 2006–2007, and 2017 (p < 0.01), but there was no significant difference among 1997–1999, 2006–2007, and 2017 (p > 0.05).

3.3.3. Changes in the Statuses of Species in the Crustacean Population

In the crustacean population, the highest P_L values in 1997–1999 belonged to Charybdis miles, while both of the highest P_L values in 2006–2007, and 2017 belonged to Solenocera crassicorni, with P_L values of 30.794%, 26.850%, and 12.802%, respectively. Similar to fish, the maximum contribution rate in each year showed a gradually decreasing trend, indicating that the dominant species status in the crustacean population gradually weakened. The total P_L of the 27 fish species listed in

Table 4. P_L values of the main species of the crustacean population in the Northern South China Sea.

Species		PL (%)
	1997–1999	2006–2007	2017
Charybdis miles (De Haan, 1835)	30.794	1.411	12.417
Portunus sanguinolentus (Herbst, 1783)	1.545	25.784	6.106
Charybdis feriatus (Linnaeus, 1758)	6.403	15.663	2.921
Solenocera crassicornis (H. Milne Edwards, 1837)	0.923	26.850	12.802
Portunus argentatus (Alcock, 1899)	15.197	0.868	3.093
Parapenaeus fissuroides Crosnier, 1986	8.851	0.169	—
Portunus gracilimanus (Stimpson, 1858)	0.026	0.046	5.836
Charybdis variegate (Fabricius, 1798)	0.010	0.030	5.141
Metapenaeopsis barbata (De Haan, 1844)	2.479	0.034	5.019
Heterocarpoides laevicarina (Bate, 1888)	4.226	—	—
Metapenaeopsis palmensis (Haswell, 1879)	0.156	0.498	3.509
Dromia dehaani Rathbun, 1923	0.008	0.079	3.301
Calappa philargius (Linnaeus, 1758)	0.670	2.391	3.177
Parapenaeopsis hardwickii (Miers, 1878)	—	0.026	3.130
Ibacus ciliatus (von Siebold, 1824)	1.627	3.112	—
Oratosquilla oratoria (De Haan, 1844)	0.034	2.966	1.500
Charybdis japonica (A. Milne-Edwards, 1861)	0.015	2.826	1.678
Portunus haanii (Stimpson, 1858)	2.620	2.107	1.842
Solenocera koelbeli De Man, 1911	2.511	0.012	—
Trachypenaeus longipes (Paulson, 1875)	2.404	0.129	0.278
Portunus hastatoides Fabricius, 1798	2.340	0.003	0.701
Metapenaeus affinis (H. Milne Edwards, 1837)	—	2.269	0.443
Philyra pisum De Haan, 1841	—	—	2.185
Charybdis truncate (Fabricius, 1798)	2.066	0.306	2.016
Harpiosquilla harpax (de Haan, 1844)	—	1.511	1.988
Oratosquilla nepa (Serville & Guérin, 1828)	0.020	1.042	0.265
Portunus trituberculatus (Miers, 1876)	0.417	0.939	0.966
Other species	14.657	8.930	19.687
Total	100	100	100

Note: “—” indicates that no data were recorded in the trawling survey.

accounted for 85.343%, 91.070%, and 80.313% of the total P_L of the crustacean population in 1997–1999, 2006–2007, and 2017, respectively. It was proven that these 27 species were the main ones maintaining the stability of the crustacean population structure in the northern South China Sea from 1997 to 2017.

Among the 27 species of crustaceans, the cumulative P_L of Charybdis miles, Portunus sanguinolentus, Charybdis feriatus, Solenocera crassicornis, and Portunus argentatus accounted for 54.863%, 70.575%, and 37.338% of the total P_L of the crustacean population in 1997–1999, 2006–2007, and 2017, respectively. The P_L values of these species were higher than those of most other species each year, indicating that these five species were the dominant species of the crustacean population in the Northern South China Sea. According to the survey data, the P_L values of Charybdis miles, Portunus sanguinolentus, Charybdis feriatus, Portunus argentatus, Portunus haanii, Portunus hastatoides, Parapenaeus fissuroides, Heterocarpoides laevicarina, Ibacus ciliates, Solenocera koelbeli, and Trachypenaeus longipes decreased in general, indicating that these species gradually lost their important roles in the population structure. The total P_L values of these species decreased from 78.520% to 27.358%. Solenocera crassicornis, Portunus gracilimanus, Charybdis variegate, Metapenaeopsis barbata, Metapenaeopsis palmensis, Dromia dehaani, Calappa philargius, Parapenaeopsis hardwickii, Oratosquilla oratoria, Charybdis japonica, Philyra pisum, Charybdis truncate, Harpiosquilla harpax, Oratosquilla nepa, and Portunus trituberculatus gradually became the new dominant species of the crustacean population. The total P_L of these species increased from 6.823% to 52.512%. According to the results of the Mann-Whitney U test, there was not a significant difference (p > 0.05) among the P_L values of the main species of the crustacean population in 1997–1999, 2006–2007, and 2017.

3.3.4. Changes in the Statuses of Species in the Cephalopod Population

In the cephalopod population, the top three P_L values in 1997–1999 belonged to Loligo edulis, Loligo chinensis, and Todarodes pacificus, with P_L of 43.654%, 22.123%, and 14.080%, respectively. In 2006–2007, the top three P_L values of the cephalopod population belonged to Loligo chinensis, Loligo edulis, and Loligo duvaucelii, with P_L of 20.827%, 17.819%, and 12.146%, respectively. In 2017, the top three P_L values of the cephalopod population belonged to Loligo duvaucelii, Loligo edulis, and Loligo tagoi, with P_L of 20.658%, 17.578%, and 15.955%, respectively. Similar to fish and crustaceans, the maximum P_L of the cephalopod population showed a gradually decreasing trend, indicating that the dominant species status in the population of cephalopods gradually weakened. This weakening trend was more obvious from 1997 to 2007, but not so clear from 2007 to 2017. The total P_L of the 14 species listed in

Table 5. The P_L values of the main species of the cephalopod population in the Northern South China Sea.

Species	PL (%)
	1997–1999	2006–2007	2017
Loligo edulis Hoyle, 1885	43.654	17.819	17.578
Loligo chinensis Gray, 1849	22.123	20.827	10.663
Loligo duvaucelii Loligo Lamarck, 1798	4.277	12.146	20.658
Sepia esculenta Hoyle, 1885	4.447	5.486	4.840
Sepia lycidas Gray, 1849	1.158	3.303	0.103
Octopus variabilis (Sasaki, 1929)	0.708	2.533	1.124
Sepioteuthis lessoniana d’Orbigny, 1826	0.612	1.822	0.235
Todarodes pacificus (Steenstrup, 1880)	14.080	3.236	—
Sepia pharaonis Ehrenberg, 1831	4.794	5.536	0.025
Loligo tagoi Sasaki, 1929	0.676	0.664	15.955
Octopus vulgaris Cuvier, 1797	0.104	6.148	0.394
Octopus ocellatus Gray, 1849	0.039	2.410	3.620
Euprymna berryi Sasaki, 1929	0.299	0.213	0.725
Octopus variabilis (Sasaki, 1929)	0.113	0.693	16.753
Other species	2.919	17.163	7.327
Total	100	100	100

Note: “—” indicates that no data were recorded in the trawling survey.

accounted for 97.081%, 82.837%, and 92.673% of the total P_L of the cephalopod population in 1997–1999, 2006–2007, and 2017, respectively. These results indicate that these 14 species were the major contributors to the stability of the cephalopod population structure in the northern South China Sea from 1997 to 2017.

Among the 14 cephalopod species (Table 5), the cumulative P_L of Loligo edulis, Loligo chinensis, and Loligo duvaucelii accounted for 70.053%, 50.793%, and 48.899% of the total P_L of the cephalopod population in 1997–1999, 2006–2007, and 2017, respectively. Although the P_L values of these three species showed a downward trend, they were generally higher than those of most other species each year, indicating that these three species were the dominant cephalopods in the Northern South China Sea. According to the survey data, the P_L values of Loligo edulis, Loligo chinensis, Sepia esculenta, Sepia lycidas, Todarodes pacificus, and Octopus variabilis decreased in general, indicating that these species gradually lost their important roles in the population structure. The total P_L values of these species decreased from 77.598% to 34.962%. Loligo duvaucelii, Loligo tagoi, Octopus ocellatus, Euprymna berryi, and Octopus variabilis gradually became the new dominant species of the cephalopod population. The total P_L of these species increased from 19.483% to 57.711%. According to the results of the Mann-Whitney U test, there was not a significant difference (p > 0.05) among the P_L values of the main species of the cephalopod population in 1997–1999, 2006–2007, and 2017.

4. Discussion

This study was based on trawl survey data from the South China Sea, using eco-exergy theory to study the community structure changes in the nekton in the northern South China Sea. The marine ecosystem contains many ecological elements, such as seawater, marine organisms, seabed sediments, etc. These ecological elements interact with each other to form complex system structures and ecological functions [48]. Fish is an important part of the marine ecosystem, and its capture not only reduces the number of its population but actually changes the structure of the marine ecosystem. Due to the special physical properties of the ocean, marine research is difficult, so most of the progress of marine science is based on the improvement of observation methods, and the complex composition of the marine environment and biological community makes the observation of marine biology more difficult [49]. Current technology cannot fully analyze marine ecosystem processes due to the limitations of ecosystem complexity and technical conditions. In ecological research, people often only study a whole system roughly or selectively study the parts of a system, whereby it is impossible to obtain accurate eco-exergy values. Researchers can only calculate the approximate eco-exergy value of a system on the basis of observation results [50]. Nevertheless, as an important objective function, eco-exergy theory still has some advantages in ecosystem research [51]. Eco-exergy theory has been widely applied in the environmental monitoring and health status evaluation of aquatic ecosystems [52,53]. Eco-exergy theory uses the sum of the product of the genetic information of each species in a system and its biomass calorific value as a measure of the thermodynamic distance away from the environmental equilibrium state and the degree of organization of the system, which can reflect the energy and genetic information that is not considered in classical indices such as biomass and biodiversity [54,55]. In addition, a system’s function and efficiency can be reflected in combination with thermodynamic indices using entropy and energy analysis methods [56,57]. Therefore, the application of eco-exergy theory and methods to the study of ecosystem dynamics is expected to reveal not only the universal law of biothermodynamics in the process of ecosystem succession and development but also the dynamic change law of the composition structure of species of different evolutionary levels in the process of ecosystem succession and development [58].

The E_X and E_Xsp of the nekton in the Northern South China Sea decreased significantly in 1964–1965, 1997–1999, 2006–2007, and 2017, indicating that the degree of orderliness, organization, and stability of the nekton community system decreased. The decrease showed a nonlinear function, with the community structure tending to be disordered and simplified. From 1964 to 2017, both the E_X and E_Xsp of the fish populations showed decreasing trends, indicating that the stability and complexity of the fish populations in the northern South China Sea weakened, and the genetic information per unit of biomass decreased. The average C value of the fish populations decreased by 16.8% from 0.952 in 1964 to 0.792 in 2017. The individual biomass of fish in 2006–2007 was significantly smaller than that in 1964–1965, and the fish tended to be miniaturized, which was a manifestation of unhealthy ecology. The E_X considering the chemical energy stored in biomass and the information embodied in genes can be used to indicate the level of ecosystem health and development. Therefore, the E_X index of the two surveys, as mentioned above, were quite different. According to the results of the two surveys, this difference is in line with reality.

The increase in E_X and the decrease in E_Xsp from 1997 to 2017 indicate that the structural stability of the crustacean population increased but the complexity decreased; that is, the genetic information contained in a unit of biomass decreased. The average C value of the crustacean population decreased 115.31% from 3.029 in 1997 to 2.566 in 2017. From 1997 to 2017, both the E_X and E_Xsp of the cephalopod populations showed increasing trends, indicating that the stability and complexity of the cephalopod population structure increased; that is, the genetic information per unit of biomass increased. In addition, the average C value of the cephalopod population increased by 57.57% from 2.434 in 1997 to 3.835 in 2017. Jorgensen believed that, for a thermodynamic system far from the equilibrium state, the increase in E_X storage runs through the development process of the whole ecosystem. In the process of the development and evolution of the ecosystem, it always tends to develop in the direction of enhancing its own stability [59]. In this study, with the declines in the E_X and E_Xsp of the fish population, the overall E_X and E_Xsp of the nekton showed a downward trend, indicating that the fish population contained the main species, maintaining the stability and order of the nekton community structure in the northern South China Sea. However, the decline in the E_X and E_Xsp of the fish population also indicated that the fish population’s role in maintaining the stability and complexity of the nekton community structure gradually weakened. At the same time, the E_X values of crustaceans and cephalopods and the E_Xsp values of cephalopods showed upward trends, indicating that the contribution of crustaceans and cephalopods to maintaining the stability and complexity of the nekton community in the northern South China Sea gradually increased. We speculate that this was an adjustment strategy made by the nekton community to enhance its own stability in the development process after being affected by human overfishing and ecological environment deterioration.

Considering that the biomass of fishery resources increased from 1997 to 2007, the E_X values of fish, crustaceans, and cephalopods showed increasing trends from 1997 to 2007, which may have been related to the fishery resource conservation measures adopted by the Chinese government in the South China Sea. In 1999, the South China Sea began the policy of a summer fishing moratorium [60]. Since 2002, provinces along the northern coast of the South China Sea have carried out the large-scale construction of artificial reefs [61]. Since 2004, provinces along the northern coast of the South China Sea have implemented fishery stock enhancements [62]. Studies have highlighted the obvious conservation and proliferation effects of the policy of the summer fishing moratorium, the construction of artificial reefs, and fishery stock enhancement [63,64,65]. These measures have slowed the resource declines of the nekton community in the northern South China Sea. From 2007 to 2017, the E_X and E_Xsp values of fish, crustaceans, and cephalopods showed downward trends, which may have been related to the continuous increase in fishing intensity in the Northern South China Sea [66].

In marine ecosystems, the trophic levels of fish are high in the food web [67,68]. Fish with high trophic levels are usually important fishery resources, which can reflect the exploitation degree of marine fishery resources. In over-exploited waters, the average body length of fish decreases, individual maturity is advanced, and the trophic level decreases [69]. The results of this study showed that the average trophic level of fish showed a downward trend in the four surveys, which indicates that there was overexploitation of economic fishery resources in the northern part of the South China Sea. Fish, crustaceans, and cephalopods have different growth processes, but they are closely related. Some kinds of crustaceans and cephalopods are food objects for fish [67]. The decreases in the E_X and E_Xsp of fish indicate that there is a decreasing number of fish in the nekton community and, therefore, less predation pressure on certain crustaceans and cephalopods. While the E_X and E_Xsp decreased in the nekton in the northern South China Sea, the E_X and E_Xsp values increased in the crustacean and cephalopod communities compared to fish.

In terms of the current catch structure in the northern South China Sea, the main catch object has changed from Lutjanus sanguineus, Gymnocranius griseus, and Pomadasys kaakan in the 1960s to Parargyrops edita, Trachurus japonicas, Decapterus maruadsi, and Nemipterus virgatus [70]. This indicates that species such as Parargyrops edita and Trachurus japonicas have replaced Lutjanus sanguineus and Gymnocranius griseus as the main species of fish in the northern South China Sea, which is consistent with the conclusion of this study that the P_L values of Lutjanus sanguineus and Gymnocranius griseus gradually decreased while the P_L values of Parargyrops edita and Trachurus japonicas gradually increased. This is consistent with the basic characteristics of the current marine ecosystem in the northern South China Sea; that is, the ecosystem is dominated by species with short life cycles, strong fertility, small individuals, and poor competitiveness (r-type species) [19]. In addition, the P_C values of crustaceans and cephalopods showed increasing trends, indicating that, after decades of intensive fishing, the species of the nekton community have changed significantly, and the fishery objects in the northern South China Sea have shifted from traditional carnivorous fish to small fish and invertebrates that feed on plankton [71]. In the northern South China Sea, the dominant position of the nekton with a high trophic level, large individuals, and a long cycle declined [72], leading to the gradual change in the dominant species from k-type species to r-type species. This replacement led to the simplification of the topological structure of the food web and increased the vulnerability of the community structure to some extent. The changes in the community structure of the nekton in the northern South China Sea are consistent with the changes in the East China Sea [73] and the Bohai Sea [74].

Marine ecosystems have high openness, complex species composition and distribution, and complex interspecific interactions, which are difficult to quantify [75]. A marine ecosystem based on E_X theory, especially its dynamic development law index system, has not yet been formed. The genetic information (C value) contained in the haploid genome of a species is an important criterion for evaluating the evolutionary level of a species. However, theoretical risks such as the C value paradox have gradually attracted attention in the process of application [76]. In addition, the lack of C value data for species is another obstacle restricting the application of ecological exergy theory. So far, millions of species have been discovered, but researchers have only measured the C values of some species, which is far from enough to meet the needs of scientific research.

In light of the decline in offshore fishery resources, the decreases in E_X and E_Xsp, and the simplification of the community structure in the South China Sea, we suggest that the policy of reducing fishing intensity should be strictly implemented, the education and training of traditional fishermen should be strengthened, employment space should be created for traditional fishermen, and fishery resource conservation measures such as the summer fishing moratorium, fishery resource enhancement, fishing intensity control, and the construction of marine ranching should continue to be implemented. Artificial habitat restoration is an important way to restore marine fishery resources, such as artificial reef construction, seaweed farm construction, and oyster and coral reef construction [77].

5. Conclusions

This study evaluated, for the first time, the dynamics of the nekton community structure in the northern South China Sea by means of eco-exergy theory based on trawl net survey data from 1964 to 2017. The total mean resource density of the nekton showed an overall declining trend, decreasing 4.12-fold. In the 53 years from 1964 to 2017, the E_X and E_Xsp of the nekton community decreased 13.28-fold and 1.42-fold, respectively. The community structure of the nekton community tended to be disordered and simplified. Fish populations remained the major contributors to the E_X and E_Xsp of the nekton communities; however, their role in maintaining the stability and complexity of the community structure gradually weakened. Meanwhile, the proportion of E_X values of crustaceans and cephalopods in the nekton community showed an upward trend. The proportion of crustaceans increased from 2.76% in 1997–1999 to 14.84% in 2017, while that of cephalopods increased from 3.55% to 16.67%. Crustaceans and cephalopods played an increasing role in the stability and complexity of the fishery resource structure in the northern South China Sea.

At present, the nekton in the northern South China Sea is dominated by species with short life cycles, strong fecundity, small individuals, and poor competitiveness. After decades of high-intensity fishing, the species replacement in the nekton has become very obvious, with the dominant species in the ecosystem gradually changing from k-type species to r-type species. We suggest that the policy of reducing fishing intensity should be strictly implemented, the education and training of traditional fishermen should be strengthened, employment space should be created for traditional fishermen, and fishery resource conservation measures such as the summer fishing moratorium, fishery enhancement, fishing intensity control, the construction of marine ranching, and artificial habitat restoration should continue to be implemented.

In the future study on the relationship between marine ecosystem dynamics and marine fishery dynamics, we can consider the key species, important species, and biological community levels to cross-synthesize physical oceanography, chemical oceanography, biological oceanography, and resource ecology. The basic structure of the food web, food quantitative relationship between main predators and prey at different life stages, energy budget characteristics, particle size spectrum and energy spectrum, ecological conversion efficiency, and their influencing factors were studied to establish nutritive dynamics models of the food web with different ecological characteristics. To study the effects of fishing, eutrophication, and other important human activities on community structure change and resource reproduction, and to explore the alternation rule and supplement mechanism of dominant species of biological resources in combination with the study of food web and population dynamics.