Dietary Composition of Big Head Croaker, Collichthys lucidus, in the Early Stage of the “10-Year Fishing Ban” Policy

Abstract

Big head croaker (Collichthys lucidus) is a dominant fish species in the Yangtze River estuary, with significant economic and ecological value in the local ecosystem. In this study, the dietary composition of big head croaker in the Yangtze River estuary from 2022 to 2023 was determined using stomach content analysis. Statistical methods such as cluster analysis and canonical correspondence analysis were also applied to study the ontogenetic variation in the feeding habits of big head croaker and their relationships with environmental factors. The results indicated that big head croaker in the Yangtze River estuary fed primarily on 15 prey groups and 33 prey species. Copepods were the dominant prey group, followed by mysids, shrimp, and fish. The dominant prey species included Acanthomysis longirostris, Neomysis awatschensis, and Calanus sinicus. Compared with historical studies, the proportion of large prey such as fish and crustaceans in the diet of big head croaker has increased since the implementation of the “10-Year Fishing Ban” on the Yangtze River, which reflects the improved aquatic habitat for organisms in the Yangtze River estuary to some extent. The feeding habits of big head croaker exhibited clear ontogenetic and seasonal variations. The empty stomach rate gradually decreased as the body size of big head croaker increased and their main prey shifted from small individuals such as Acetes chinensis and A. longirostris to larger individual fishes and Brachyura. In addition, big head croaker primarily fed on N. awatschensis in spring, A. longirostris in summer and autumn, and Acrocalanus gibber in winter. Canonical correspondence analysis indicated that salinity and length were the factors most strongly correlated with the feeding habits of big head croaker, followed by latitude and longitude.

1. Introduction

Understanding the feeding habits of Teleostei is crucial for assessing the roles of Teleostei in ecosystems and energy flow through food webs [1]. Various methods can be used for analyzing feeding habits, such as stomach content analysis [2,3], stable isotope techniques [1], fatty acid analysis [4], and high-throughput sequencing [5]. In particular, stomach content analysis is the most direct method for obtaining individual feeding information in nutritional dynamics research [2,6]. Prey species can be identified by analyzing the contents of fish stomachs and they directly reflect the compositions of fish diets and their nutritional status. This method is also useful for studying material cycles within food chains and webs in ecosystems and it is considered the standard approach for fish diet analysis [6,7].

The Yangtze River estuary features rich trophic resources, high productivity, and diverse environmental gradients, serving as an essential spawning, nursery, feeding, and migratory corridor for fish [8,9]. However, in recent years, due to the long-term and high-intensity fishing pressure, the population of big head croaker and other fish species has generally declined in the Yangtze River estuary [10]. Consequently, China officially implemented a “10-Year Fishing Ban” policy in 2021 to protect the aquatic biological resources and diversity in the Yangtze River basin. Aquatic biological resources in the estuary exhibited various responses to the removal of fishing pressure [11], leading to changes in the trophic interactions among species. From 2017 to 2023 the resource abundance of omnivorous fish in the Yangtze River estuary dropped from 31.02% pre-ban to 15.36% post-ban. For carnivorous fish, it rose from 58.36% pre-ban to 83.77% post-ban. This indicates a significant shift in the proportions of feeding and ecological types of fish in the area due to the fishing ban [12]. Understanding the feeding habits of fish after the “10-Year Fishing Ban” is helpful for identifying the mechanisms that might allow the fishing ban policy to affect aquatic organisms and better assess the ecological effects of the policy.

Big head croaker (Collichthys lucidus) is widely distributed in the Yellow Sea, Bohai Sea, and East China Sea, and it is a dominant species in the Yangtze River estuary [13]. This species is characterized by its wide tolerance of differences in temperature and salinity; they typically migrate to estuaries to spawn as water temperatures rise in spring and summer, with peak spawning occurring from April through June [14]. Big head croaker is a typical carnivorous fish in the secondary consumer trophic level. Based on historical research, its diet consists of a diverse range of marine species [15]. In addition, big head croaker is the main prey species of many top predators such as hairtail and Bombay duck [16]. Therefore, the big head croaker plays an important role in the trophic dynamics of the Yangtze River estuary ecosystem.

Recent research into big head croaker has mainly focused on morphological characteristics, nutritional components, and community features [17,18,19,20,21,22]. Since 2013–2014, studies have applied methods such as isotopic analysis to investigate the feeding habits of big head croaker in the East China Sea, Yellow Sea, and Han River estuary [19,23,24]. Research into the feeding habits of big head croaker in the Yangtze River estuary was mainly conducted during 2013–2014 [10]. There have been no recent studies of the feeding habits of big head croaker following the fishing ban, which hinders analysis of the ecological effects of the ban.

In the present study, stomach content analysis was applied to examine the dietary composition of big head croaker in the Yangtze River estuary from 2022 to 2023, as well as to investigate the relationships between their dietary composition and factors such as the predator body size and season. The objectives of this study were: (1) to understand the current dietary characteristics of big head croaker in the Yangtze River estuary; (2) to explore changes in their feeding habits since the fishing ban based on comparisons with historical data; and (3) to provide a reference for studying the food web in the Yangtze River estuary.

2. Materials and Methods

2.1. Sample Collection and Analysis

Big head croaker samples were collected during fishery resource surveys conducted in the Yangtze River estuary across four seasons (March to May was defined as spring, June to August was summer, September to November was autumn, and December to February was winter) from July 2022 to May 2023 (Figure 1), with a total of 18 fixed stations set in the area. Bottom trawl surveys were conducted to collect fish samples. The surveys were performed using a double-bag bottom trawl, with a mouth width of 6 m, height of 2 m, and mesh size of 20 mm. The average trawling speed at each station was 2 Knots and the average trawling time was 30 min. A portable multi-parameter water quality meter (WTW Multi 3430) as well as shipborne echo sounder were used to simultaneously measure environmental factors (sea surface temperature, sea surface salinity, sea surface dissolved oxygen, water depth, etc.) at each survey station. Some sampling stations were located near the shoreline, primarily to avoid restricting the shipping channel and to focus on the shallow areas where higher fish diversity was typically found. All big head croaker samples were collected and preserved with ice. Biological parameters such as body length and weight were measured in the laboratory according to the standards of the “Marine Survey Specifications Part 6: Marine Biological Survey” [25], and the stomachs were removed and stored in a freezer at –20 °C. In total, 531 stomach samples were collected for subsequent analysis.

2.2. Sample Analysis

To conduct stomach content analysis, the stomach samples were thawed and then cut open with scissors to remove any prey items inside. All prey items were identified and counted under a Jiangnan JSZ6S.stereoscopic microscope. Intact species organisms were identified directly, whereas damaged species were identified based on indigestible parts, such as otoliths, vertebrae, scales, chelae, and jaw teeth [2,6]. All prey items were identified to the lowest taxonomic unit. The mass of each prey item was measured using a precision electronic balance (OHAUSPWN85ZH, accuracy = 0.01 mg), where as much surface moisture as possible was absorbed from the prey item with absorbent paper before weighing.

2.3. Data Processing

Among the 531 stomach samples analyzed in this study, 392 were found to contain prey items, with an empty stomach rate of 26.18% (

Table 1. The number of big head croaker stomach samples in each season and body size groups.

Size Class/mm	<60	60–80	80–100	100–120	120–140	>140
Spr	7(2)	10(3)	21	17(2)	22	11
Sum	43(12)	32(9)	13(1)	9(2)	9(1)	3
Aut	4(2)	16(3)	29(10)	21(7)	21(12)	9(4)
Win	4(3)	65(19)	67(24)	21(3)	14(2)	4(1)

Number in bracket indicated empty stomachs, in the total of 531 stomachs, 59 samples were excluded due to the lack of body length information.

). The feeding intensity of big head croaker was determined based on the stomach fullness index and empty stomach rate [7]. The importance of prey items was analyzed using the percentage of prey weight (W%), percentage of number (N%), frequency of occurrence (F%), index of relative importance (IRI), and percentage of IRI (IRI%), which were calculated as follows:

$$\mathrm{Stomach} \mathrm{Fullness} \mathrm{Index}={\displaystyle \frac{\mathrm{T}\mathrm{o}\mathrm{t}\mathrm{a}\mathrm{l} \mathrm{w}\mathrm{e}\mathrm{i}\mathrm{g}\mathrm{h}\mathrm{t} \mathrm{o}\mathrm{f} \mathrm{p}\mathrm{r}\mathrm{e}\mathrm{y} \mathrm{o}\mathrm{r}\mathrm{g}\mathrm{a}\mathrm{n}\mathrm{i}\mathrm{s}\mathrm{m}\mathrm{s} \mathrm{i}\mathrm{n} \mathrm{f}\mathrm{o}\mathrm{o}\mathrm{d} \mathrm{i}\mathrm{t}\mathrm{e}\mathrm{m}\mathrm{s}}{\mathrm{T}\mathrm{o}\mathrm{t}\mathrm{a}\mathrm{l} \mathrm{n}\mathrm{u}\mathrm{m}\mathrm{b}\mathrm{e}\mathrm{r} \mathrm{o}\mathrm{f} \mathrm{a}\mathrm{l}\mathrm{l} \mathrm{f}\mathrm{o}\mathrm{o}\mathrm{d} \mathrm{i}\mathrm{t}\mathrm{e}\mathrm{m}\mathrm{s}}} \times 10000$$

(1)

$$\mathrm{Empty} \mathrm{Stomach} \mathrm{Rate}={\displaystyle \frac{\mathrm{N}\mathrm{u}\mathrm{m}\mathrm{b}\mathrm{e}\mathrm{r} \mathrm{o}\mathrm{f} \mathrm{e}\mathrm{m}\mathrm{p}\mathrm{t}\mathrm{y} \mathrm{s}\mathrm{t}\mathrm{o}\mathrm{m}\mathrm{a}\mathrm{c}\mathrm{h}\mathrm{s}}{\mathrm{T}\mathrm{o}\mathrm{t}\mathrm{a}\mathrm{l} \mathrm{n}\mathrm{u}\mathrm{m}\mathrm{b}\mathrm{e}\mathrm{r} \mathrm{o}\mathrm{f} \mathrm{a}\mathrm{l}\mathrm{l} \mathrm{s}\mathrm{t}\mathrm{o}\mathrm{m}\mathrm{a}\mathrm{c}\mathrm{h}\mathrm{s}}} \times 100\%$$

(2)

$$\mathrm{Weight} \mathrm{Percentage} (\mathrm{W}\%)={\displaystyle \frac{\mathrm{N}\mathrm{u}\mathrm{m}\mathrm{b}\mathrm{e}\mathrm{r} \mathrm{o}\mathrm{f} \mathrm{p}\mathrm{a}\mathrm{r}\mathrm{t}\mathrm{i}\mathrm{c}\mathrm{u}\mathrm{l}\mathrm{a}\mathrm{r} \mathrm{f}\mathrm{o}\mathrm{o}\mathrm{d} \mathrm{i}\mathrm{t}\mathrm{e}\mathrm{m}}{\mathrm{T}\mathrm{o}\mathrm{t}\mathrm{a}\mathrm{l} \mathrm{n}\mathrm{u}\mathrm{m}\mathrm{b}\mathrm{e}\mathrm{r} \mathrm{o}\mathrm{f} \mathrm{a}\mathrm{l}\mathrm{l} \mathrm{f}\mathrm{o}\mathrm{o}\mathrm{d} \mathrm{i}\mathrm{t}\mathrm{e}\mathrm{m}\mathrm{s}}} \times 100\%$$

(3)

$$\mathrm{Number} \mathrm{Percentage} (\mathrm{N}\%)={\displaystyle \frac{\mathrm{B}\mathrm{i}\mathrm{o}\mathrm{l}\mathrm{o}\mathrm{g}\mathrm{i}\mathrm{c}\mathrm{a}\mathrm{l} \mathrm{w}\mathrm{e}\mathrm{i}\mathrm{g}\mathrm{h}\mathrm{t} \mathrm{o}\mathrm{f} \mathrm{p}\mathrm{a}\mathrm{r}\mathrm{t}\mathrm{i}\mathrm{c}\mathrm{u}\mathrm{l}\mathrm{a}\mathrm{r} \mathrm{f}\mathrm{o}\mathrm{o}\mathrm{d} \mathrm{i}\mathrm{t}\mathrm{e}\mathrm{m}}{\mathrm{T}\mathrm{o}\mathrm{t}\mathrm{a}\mathrm{l} \mathrm{w}\mathrm{e}\mathrm{i}\mathrm{g}\mathrm{h}\mathrm{t} \mathrm{o}\mathrm{f} \mathrm{a}\mathrm{l}\mathrm{l} \mathrm{f}\mathrm{o}\mathrm{o}\mathrm{d} \mathrm{i}\mathrm{t}\mathrm{e}\mathrm{m}\mathrm{s}}} \times 100\%$$

(4)

$$\mathrm{Frequency} \mathrm{of} \mathrm{Occurrence} (\mathrm{F}\%)={\displaystyle \frac{\mathrm{F}\mathrm{r}\mathrm{e}\mathrm{q}\mathrm{u}\mathrm{e}\mathrm{n}\mathrm{c}\mathrm{y} \mathrm{o}\mathrm{f} \mathrm{o}\mathrm{c}\mathrm{c}\mathrm{u}\mathrm{r}\mathrm{r}\mathrm{e}\mathrm{n}\mathrm{c}\mathrm{e} \mathrm{o}\mathrm{f} \mathrm{p}\mathrm{a}\mathrm{r}\mathrm{t}\mathrm{i}\mathrm{c}\mathrm{u}\mathrm{l}\mathrm{a}\mathrm{r} \mathrm{f}\mathrm{o}\mathrm{o}\mathrm{d} \mathrm{i}\mathrm{t}\mathrm{e}\mathrm{m}}{\mathrm{N}\mathrm{u}\mathrm{m}\mathrm{b}\mathrm{e}\mathrm{r} \mathrm{o}\mathrm{f} \mathrm{s}\mathrm{t}\mathrm{o}\mathrm{m}\mathrm{a}\mathrm{c}\mathrm{h}\mathrm{s} \mathrm{c}\mathrm{o}\mathrm{n}\mathrm{t}\mathrm{a}\mathrm{i}\mathrm{n}\mathrm{i}\mathrm{n}\mathrm{g} \mathrm{f}\mathrm{o}\mathrm{o}\mathrm{d} \mathrm{i}\mathrm{t}\mathrm{e}\mathrm{m}}} \times 100\%$$

(5)

Index of Relative Importance (IRI) = F% × (W%+ N%)

(6)

$$\mathrm{Percentage} \mathrm{of} \mathrm{Index} \mathrm{of} \mathrm{Relative} \mathrm{Importance} (\mathrm{IRI}\%)={\displaystyle \frac{\mathrm{I}\mathrm{R}\mathrm{I}}{\mathsf{\Sigma }\mathrm{I}\mathrm{R}\mathrm{I}}} \times 100$$

(7)

Based on a size interval of 20 mm, big head croaker were divided into six body length groups: <60 mm, 60–80 mm, 80–100 mm, 100–120 mm, 120–140 mm, and >140 mm. Prey species were classified into 14 groups based on their taxonomic characteristics as: Teleostei, Brachyura, Decapoda, Euphausiacea, Mysidacea, Luciferidae, Bivalvia, Amphipoda, Isopoda, pelagic larvae, Cladocera, copepods, Polychaeta, and Nematoda. The Kruskal–Wallis test was applied to analyze ontogenetic variations in the stomach fullness index of big head croaker (α = 0.05). Cluster analysis was used to compare the feeding habits of big head croaker in different body length groups. The W% values for each prey group were square-root transformed before analysis. The Bray–Curtis similarity matrix was calculated for the food composition in each body length group and used for cluster analysis. The Kruskal–Wallis test was conducted using R language and cluster analysis was performed using Primer 5.0 software.

Canonical correspondence analysis (CCA) can reveal the potential relationships between environmental factors and the dietary compositions of Teleostei [6,7]. CCA requires the construction of a species matrix and explanatory variable matrix. In this study, the species data matrix was constructed based on the W% value for each prey item. Before analysis, unidentifiable prey and rare prey that appeared less than five times were removed to exclude their influence on the results. The explanatory variable matrix contained the predator body length, sampling season, longitude, latitude, sea water temperature, depth, salinity, and dissolved oxygen. Environmental data that did not satisfy the requirement for a normal distribution (except for season) were log transformed (lg(X + 1)) to stabilize the variance and reduce the impacts of extreme values [7]. Variance inflation factor (VIF) values were calculated to examine the collinearity among explanatory variables. Variables with high VIF values (>10) were highly correlated with other variables [26]. Variables were omitted from the CCA test if they had a high VIF value and low biological significance. CCA was conducted using the “vegan” package in R 4.3.2.

3. Results and Analysis

3.1. Dietary Composition of Big Head Croaker in the Yangtze River Estuary

Stomach content analysis showed that big head croaker in the Yangtze River estuary consumed items from 15 prey groups and 33 prey species between 2022 and 2023 (

Table 2. Diet composition of big head croaker at the Yangtze River estuary.

Prey Item	F%	W%	N%	IRI%
Teleostei	2.80	44.35	1.22	4.10
Coilia nasus	0.22	4.75	0.09	0.08
Harpadon nehereus	1.08	27.42	0.47	2.44
Unidentified fish	1.51	12.18	0.66	1.57
Brachyura	1.94	1.18	1.03	0.11
Charybdis japonica	0.22	0.18	0.09	0.00
Neoeriocheir leptognathus	0.86	0.39	0.56	0.07
Portunus sp.	0.43	0.03	0.19	0.01
Xiphonectes hastatoides	0.43	0.58	0.19	0.03
Decapoda	22.41	35.69	12.78	13.93
Acetes chinensis	3.66	8.40	1.97	3.09
Alpheus japonicus	0.43	2.64	0.19	0.10
Exopalaemon annandalei	1.51	4.68	0.75	0.67
E. carinicauda	1.51	3.94	1.03	0.61
Leptochela gracilis	0.65	0.13	0.38	0.03
Macrobrachium nipponense	0.43	0.00	0.19	0.01
Palaemon gravieri	2.80	6.95	1.41	1.90
P. macrodactylus	0.22	0.24	0.09	0.01
Parapenaeopsis tenella	1.72	5.21	1.03	0.87
Plesionika izumiae	0.43	0.01	0.19	0.01
Unidentified Decapod	9.05	3.48	5.55	6.64
Euphausiacea	6.25	3.30	3.29	2.51
Pseudeuphausia sinica	5.17	3.27	2.54	2.44
Unidentified Euphausiacea	1.08	0.03	0.75	0.07
Mysidcea	35.78	14.30	35.34	59.00
Acanthomysis longirostris	20.69	5.06	15.70	34.90
Neomysis awatschensis	10.99	9.14	17.11	23.43
Siriella sinensis	0.65	0.00	0.28	0.02
unidentified Mysidcea	3.45	0.10	2.26	0.66
Luciferidae	0.22	0.00	0.09	0.00
Unidentified Luciferidae	0.22	0.00	0.09	0.00
Bivalvia	0.22	0.00	0.09	0.00
Trapezium liratum	0.22	0.00	0.09	0.00
Amphipoda	0.65	0.33	0.38	0.02
Corphium volutator	0.22	0.01	0.09	0.00
Oxycephalus clausi	0.43	0.31	0.28	0.02
Isopoda	1.29	0.22	0.56	0.05
Synidotea laecidorsalis	1.08	0.11	0.47	0.05
Unidentified Bosmina	0.22	0.11	0.09	0.00
Pelagic larvae	0.22	0.06	0.19	0.00
Megalopa larvae	0.22	0.06	0.19	0.00
Cladocera	0.86	0.00	0.47	0.03
Penilia avirostris	0.86	0.00	0.47	0.03
Copepods	24.57	0.35	43.05	20.13
Acartia pacifica	1.08	0.00	0.85	0.07
Acrocalanus gibber	8.84	0.10	14.47	10.46
Calanus sinicus	6.03	0.07	11.28	5.57
Paracalanus aculeatus	3.88	0.10	8.65	2.76
P. parvus	2.37	0.06	4.79	0.93
Schmackeria poplesia	0.22	0.01	1.22	0.02
Unidentified copepods	2.16	0.01	1.79	0.31
Polychaeta	0.65	0.07	0.28	0.02
Unidentified Polychaeta	0.65	0.07	0.28	0.02
Nematoda	0.65	0.01	0.28	0.02
Caenorhabditis elegans	0.65	0.01	0.28	0.02
Others	1.51	0.15	0.94	0.08
Scale armor	1.08	0.00	0.75	0.07
Unidentified prey	0.43	0.14	0.19	0.01

Bold items indicated prey categories.

). The main prey categories were Mysidacea and copepods, followed by Decapoda and Teleostei. The highest IRI% and F% were for Acanthomysis longirostris (IRI% 34.90%, F% 20.69%). The highest W% was for Harpadon nehereus (27.42%) and the highest N% was for N. awatschensis (17.11%).

3.2. The Food Composition of Big Head Croaker Varies with Body Length

The stomach fullness index was highest in the body length group measuring < 60 mm at 32.20 (Figure 2), due to their consumption of large amounts of Palaemon gravieri. The index values for other groups were all below 10, where the body length groups measuring 120–140 mm and 100–120 mm had relatively high index values of 6.85 and 6.40, respectively. However, the empty stomach rate decreased as the body length increased, with lower empty stomach rates mainly occurring in the body length groups measuring > 160 mm and 140–160 mm. The result of Kruskal–Wallis test indicated that the changes in the stomach fullness index with body length classes were significant (p < 0.05).

Ontogenetic variations were found in the feeding habits of big head croaker in the Yangtze River estuary. In general, smaller big head croaker (<80 mm) preferred small size prey items (

Table 3. Ontogenetic variations in the percentage of weight (W%) of major prey groups in the diet of big head croaker.

Prey Group	Size Class/mm
	<60	60–80	80–100	100–120	120–140	>140
Teleostei	1.61	0.29	0.00	56.87	53.59	67.98
Brachyura	0.06	0.10	1.90	1.78	1.55	0.00
Decapoda	78.29	57.64	58.55	31.60	29.48	22.50
Euphausiacea	0.69	1.35	8.61	0.54	3.04	1.64
Mysidcea	8.25	35.77	29.44	8.93	12.07	7.79
Luciferidae	0.00	0.00	0.00	0.00	0.00	0.00
Bivalvia	0.00	0.00	0.00	0.00	0.01	0.00
Amphipoda	10.97	0.00	0.00	0.14	0.00	0.09
Isopoda	0.04	1.33	0.00	0.00	0.19	0.00
Pelagic larvae	0.00	0.00	0.00	0.02	0.00	0.00
Cladocera	0.00	0.00	0.00	0.00	0.00	0.00
Copepods	0.05	1.62	0.92	0.11	0.03	0.00
Polychaeta	0.00	0.15	0.58	0.00	0.00	0.00
Nematoda	0.00	0.00	0.00	0.00	0.03	0.00
Others	0.05	1.75	0.00	0.00	0.00	0.00

), such as Decapoda, Mysidcea, and Amphipoda, whereas large big head croaker (>100 mm) mainly fed on large size prey items, such as Teleostei. Medium-sized big head croaker (80–100 mm) consumed more Decapoda, Mysidcea, and Euphausiacea than those in the other body size groups. Big head croaker smaller than 60 mm mainly fed on Decapoda and Amphipoda, with W% values of 78.29% and 10.97%, respectively. Teleostei and Decapoda were the dominant prey items in the largest big head croaker size group (>140 mm).

Based on the Bray–Curtis similarity coefficient and using 20% similarity as the criterion, the eight body length groups of big head croaker were divided into four groups (Figure 3). In general, big head croaker with a body length less than 60 mm formed one group, which primarily fed on P. gravieri and Oxycephalus clausi. Big head croaker with body lengths of 60–100 mm had a food composition similarity of 51.75%, and they mainly fed on Parapenaeopsis tenella, A. longirostris, and N. awatschensis. The third group contained big head croaker with body lengths of 100–120 mm and they mainly fed on H. nehereus and Coilia nasus. The fourth group contained big head croaker with body lengths greater than 120 mm; the food composition similarity within this group was 65.39% and they mainly fed on H. nehereus and N. awatschensis.

3.3. Feeding Habits of Big Head Croaker Varied Among Seasons

The dietary compositions of big head croaker in the Yangtze River estuary also exhibited distinct seasonal variations. Based on IRI%, the high importance prey items were Mysidacea in both spring and summer, with IRI% values of 83.86% and 51.38%, respectively. In autumn, the dominant prey item for big head croaker was Decapoda (50.07%) and copepods (66.06%) were the dominant prey items in winter. In terms of F%, the most frequent prey species consumed by big head croaker in spring were Mysidacea, followed by copepods, with F% values of 53.03% and 23.48%, respectively. In summer, the most frequently consumed prey items were Decapoda, followed by Mysidacea, with F% values of 35.77% and 30.08%, respectively. In autumn, the most frequently consumed prey items were Mysidacea and Decapoda, with F% values of 42.42% and 40.91%, respectively. In winter, copepods had the highest F% value of 48.95% (Figure 4). In terms of W%, the prey species with the highest W% values consumed by big head croaker in spring, summer, and autumn were Decapoda, with W% values of 53.41%, 93.72%, and 46.84%, respectively. In winter, the prey item with the highest W% value was Teleostei (95.07%). In terms of N%, Mysidacea were the most frequently consumed prey species in spring, summer, and autumn, with N% values of 52.74%, 44.27%, and 42.50%, respectively. In winter, copepods had the highest N% value of 74.66%.

3.4. Relationships Between Feeding Habits of Big Head Croaker and Environmental Factors

According to the VIF test results, temperature had the highest VIF value (287.58); considering its high relationship with different seasons, the temperature was omitted in the following CCA test. Different seasons also had relatively high VIF values (13.48–17.47) but this variable was retained because it is important to study seasonal variations in fish feeding habits. The final explanatory variables were body length, water depth, salinity, dissolved oxygen, longitude, latitude, and season. CCA indicated that environmental factors explained 23.25% of the total variation in the prey of big head croaker in the Yangtze River estuary, where the first and second axes explained 62.33% of the relationships between biotic and explanatory variables.

Based on the lengths of vector line segments, salinity and body length had relatively stronger correlations with the feeding habits of big head croaker, followed by longitude and latitude. In areas with deeper water, the main prey species for big head croaker was P. sinica, whereas more C. sinicus tended to be consumed in areas at higher longitudes. At high latitudes, big head croaker tended to feed more on Paracalanus aculeatus and A. gibber. The CCA results also indicated that the feeding habits of big head croaker were closely related to the season, with preference for more Mysidacea and Decapoda in spring, and copepods in winter (Figure 5).

4. Discussion

4.1. Prey Types of Big Head Croaker

This study investigated the feeding habits of big head croaker in the Yangtze River estuary by using stomach content analysis. The results showed that from 2022 to 2023, big head croaker mainly fed on Mysidacea, copepods, Decapoda, and Teleostei in the Yangtze River estuary, where the dominant prey species were A. longirostris, N. awatschensis, and C. sinicus, indicating that big head croaker is a planktivorous fish. The feeding preference of big head croaker is closely related to its fine and sharp teeth, as well as its numerous and slender gill rakers, which facilitate the consumption of plankton [27]. In terms of the temporal variations in the feeding habits of big head croaker, the main prey of big head croaker in the Yangtze River estuary during the 1970s were small benthic fish and shrimp [28]. However, in the present study, big head croaker fed mainly on Mysidacea and copepods and similar findings were obtained by stomach content analysis in 2013 and 2014 [10]. In addition, studies of the feeding habits of big head croaker in the East China Sea during 2006–2008 [29] and 2019–2021 [23] showed that the main prey items were Euphausiacea and other planktonic organisms. The shift in the feeding habit of big head croaker from fish in 1970s to plankton after 2000s may reflect changes in the biological community structure within its habitat. The migration routes of many migratory species have been blocked since the partial obstruction caused by the Gezhouba Dam project [30] and this combined with long-term overfishing has led to significant declines in the aquatic biological resources in the Yangtze River estuary [31]. Moreover, upstream dams in the Yangtze River have altered the river’s flow velocity and volume, thereby changing the estuarine hydrological conditions and affecting the survival environment for aquatic organisms such as big head croaker [32], as well as possibly further affecting the species richness of the biological community in the estuary. Additionally, the shift in the feeding habits of big head croaker also indicated its broad diet spectrum and generalized feeding strategy, which is the main reason that it can suffer violent environmental change and keep relative high abundance in the last serval decades [10].

Moreover, the size of the big head croaker samples greatly affected the dietary analysis results. The stomach fullness index was highest in P. gravieri individuals with a body length < 60 mm. This is mainly because the big head croaker in the <60 mm body length group were mostly collected in summer and had consumed large amounts of Palaemon gravieri. As a warm temperate species, P. gravieri is more abundant in summer and autumn than in winter and spring [33]. The size of individual big head croaker has generally decreased due to high-intensity fishing pressure [20]. In the present study, most of the individual big head croaker had a body length less than 90 mm. A 1-year-old big head croaker has a body length of around 81 mm [21], which indicates that the individual big head croaker collected in this study were mainly 1-year-old juveniles. This is another reason why they tended to feed on small prey organisms.

It should be noted that after the implementation of the “10-Year Fishing Ban” policy in the Yangtze River, the proportion of fish has increased in the diet of big head croaker in the Yangtze River estuary, where the relative importance percentage of fish in their diet increased from 0.12% in 2013–2014 to 4.1% in 2022–2023. Japanese grenadier anchovy (C. nasus) was directly detected in the stomach of Yangtze River estuary big head croaker, which is consistent with the stomach content DNA analysis results for big head croaker in the Yangtze River estuary during 2021 [22]. Earlier studies (before 2021) of the feeding habits of big head croaker in the Yangtze River estuary did not detect C. nasus. The C. nasus resources were at an endangered level due to long-term overfishing [34,35]. Due to the implementation of the fishing ban policy, the population of C. nasus has grown rapidly. Dominate nekton species in Yangtze River estuary have transformed from shrimp and crab before the fishing ban to fishes such as bighead croaker and C. Nasus after fishing ban policy was implement [12]. Data based on the same survey also indicated that the relative abundance of C. nasus in the Yangtze River estuary increased about by seven times in 2023 compared with the year before the fishing ban (2019) (unpublished data). The recent high biomass of C. nasus in the Yangtze River estuary has resulted in a dietary shift in bighead croaker. It should be noted that the previous DNA signals of C. nasus detected in stomach content analyses in early study [22] may have originated from eggs or larval stages, as DNA-based methods cannot distinguish between life stages of the organism [6], which indicated that the egg and larvae of C. nasus might be potential prey items of big heat croaker. In the present study, the relative increase in the proportion of fish in the diet of big head croaker may have been affected by estimation errors due to inconsistencies in the sampling seasons and predator sizes [7], but the significant growth in the ratio of fish in the diet also reflected the recovery of Teleostei after the fishing ban policy [6]. Further studies should focus on how the fishing ban policy affects the feeding habits of fish.

4.2. Ontogenetic and Seasonal Variations in the Feeding Habits of Big Head Croaker

Fish exhibit significant differences in terms of their feeding habits among different seasons and body lengths due to the different energy requirements for growth and development [6,7,36]. The size of prey consumed by fish typically increases with their own body length [7]. In the present study, as the body length of big head croaker increased, the proportion of small prey such as copepods, Euphausiacea, and Mysidacea gradually decreased, whereas the proportion of large prey such as Teleostei, Decapoda, and Brachyura increased, mainly due to the enhanced predation capabilities of the predator. As fish grow, their feeding organs become more refined and their pursuit abilities improve, leading to an increased proportion of large, agile prey in their diet [6]. This phenomenon is consistent with “optimal foraging theory”, where in order to meet the energy needs for growth and development, a predator always tends to adopt a feeding strategy that maximizes their energy intake with minimal expenditure [37].

In terms of seasonality, big head croaker primarily fed on Decapoda and Mysidacea during the summer, but mainly copepods and a certain proportion of Mysidacea in winter, thereby reflecting the seasonal variations in the abundances of prey species in the Yangtze River estuary. The diet of big head croaker in the Yangtze River estuary was most diverse in summer, as also shown by Zhenhua et al. [38], indicating that the community structure in the Yangtze River estuary has tended to improve during the summer. In spring, big head croaker primarily fed on C. sinicus, mainly because C. sinicus is a dominant species in the spring Yangtze River estuary [39]. In addition, the proportion of fish in the diet was relatively high during winter than other seasons, mainly because of the higher occurrence frequency of its primary fish prey items, such as H. nehereus, during the winter season [40]. Therefore, the seasonal changes in the prey species of big head croaker in the Yangtze River estuary were consistent with the seasonal fluctuations in prey species in the estuarine waters, as also shown in most previous studies of the feeding habits of fish [41]. Moreover, the reproductive ecology of big head croaker might affect its seasonal dietary shift. Big head croaker tends to spawn in spring and summer [15]; the gonads occupy a relatively large portion of the body cavity of fish, often leading to reduced feeding intensity [7]. Therefore, the seasonal variations in fish feeding habits are likely the result of multiple interacting factors, which call for further comprehensive analysis.

4.3. Factors That Affected the Feeding Habits of Big Head Croaker

Environmental factors can profoundly influence the distribution patterns and population dynamics of species, and directly or indirectly affect the feeding habits of fish [42,43]. The results obtained in the present study indicated that salinity and body length were strongly correlated with the feeding habits of big head croaker in the Yangtze River estuary. As a marine fish, big head croaker exhibits high adaptability to salinity [44], and thus it is widely distributed across water bodies with different salinity levels and is a dominant species in estuarine waters [45]. However, some of the big head croaker’s prey species have narrower salinity tolerance ranges [15], leading to preferences for different types of prey in waters with different salinity levels. For example, A. gibber is an offshore copepod that tends to be distributed in waters with a higher salinity, whereas C. sinicus is a coastal copepod that prefers to be distributed in mixed brackish and freshwater water bodies [39]. Therefore, big head croaker had a relatively higher proportion of A. gibber in its diet in higher salinity waters. Latitude was correlated with other explanatory variables such as salinity and dissolved oxygen, which actually reflected the different hydrological conditions in the north and south branches of the Yangtze River estuary. The south branch of the Yangtze River estuary is greatly influenced by river runoff, whereas the north branch is affected more by tidal currents due to the low river runoff [46]. This specific geographical structure results in higher salinity and dissolved oxygen levels in the north branch compared with the south branch [47]. In both the south and north branches of the Yangtze River estuary, big head croaker fed mainly on Mysidacea, but they also consumed a significant proportion of copepods such as A. gibber and C. sinicus as prey in the north branch, which reflected the differences in the adaptability of these prey species to different salinity and dissolved oxygen levels [48,49]. By contrast, in the south branch, the proportions of shrimp and Brachyura were higher in the diet of big head croaker, such as P. tenella and Neoeriocheir leptognathus. The negative correlation between big head croaker body length and latitude also indicated that larger croaker tend to occurred in lower-latitude areas (south branch of Yangtze River estuary). This phenomenon is likely attributable to the relatively higher prey availability in brackish-freshwater mixing zone. Finally, the relationship between prey item Pseudeuphausia sinica and depth indicated that the big head croaker tend to consume more P. sinica in the depth area, which is mainly because P. sinica preferred a relatively deep water habitat in the study area. P. sinica is a large marine zooplankton that are widely distributed in the offshore waters of the Yangtze River estuary, where the water depth was generally greater [50].

5. Conclusions

In conclusion, the big head croaker in the Yangtze River estuary mainly fed on 15 prey groups and 33 prey species, where Mysidacea was the most important prey group, followed by copepods, shrimps, and Teleostei. The dominant prey species included A. longirostris, N. awatschensis, and C. sinicus. Compared with historical studies, the dominant prey species for big head croaker have shifted from Teleostei in the 1990s to planktonic animals at present. However, since the implementation of the Yangtze River “10-Year Fishing Ban” policy, big head croaker have begun to consume more large prey, such as fish and crustaceans, which reflects the improved ecological environment quality of the Yangtze River estuary.

The diet of big head croaker in the Yangtze River estuary changed significantly with their growth. As the body length increased, the number of prey groups gradually increased in the diet and the proportions of large prey such as Teleostei and Brachyura also increased. The proportions of small prey such as copepods and Mysid shrimps gradually decreased. The diet of big head croaker in the Yangtze River estuary also exhibited significant seasonal variation, where they fed mainly on Mysid shrimps in spring and summer, shrimps in autumn, and copepods in winter.

Salinity and body length were most strongly correlated with the prey composition for big head croaker, followed by longitude and latitude. The main prey was P. sinica in deeper water areas and C. sinicus in higher longitude areas. In high latitude areas, big head croaker tended to feed more on P. aculeatus and A. gibber. In both the southern and northern branches of the Yangtze River estuary, big head croaker mainly fed on Mysidacea. In the northern branch, the most common prey species were A. gibber, C. sinicus, and other copepods. In the southern branch, the proportions were higher of shrimps and Brachyura, such as P. tenella and N. leptognathus.

In addition, a clear increase was found in the rate of C. nasus fish consumption after the implementation of the “10-Year Fishing Ban” policy.