Age, Growth, Sex Composition, and Diet of the Burbot, Lota lota, the Only Freshwater Species of the Family Lotidae in the Amur (Heilongjiang) River, Northeast China

Abstract

Information about the population structure, including the age and sex composition, growth characteristics, and diet of fish, is essential for the conservation and sustainable exploitation of fish stock. The burbot, Lota lota, is the only freshwater species of the family Lotidae in the Amur (Heilongjiang) River catchment located in northeastern China. Information on the biological characteristics and data on the population structure of this fish from the Amur River are scarce. To study these factors in burbot, Lota lota, in the Amur River of China, 749 specimens from four sampling areas were taken and analyzed in October 2022, January 2023, and May 2023. The ages of the sampled fish ranged from 1+ to 7+ years. The female/male ratio was 1.04:1, and body length and mass varied from 175 to 595 mm and 73.5 to 1958.7 g, respectively. The length–weight regression parameter b value was estimated as 2.80. The parameters of the von Bertalanffy growth model were L_∞ = 596, K = 0.221, and t₀ = −0.771 for all sampled fish; L_∞ = 625, K = 0.208, and t₀ = −0.756 for females; and L_∞ = 584, K = 0.219, and t₀ = −0.980 for males. The analysis of the stomach contents showed fish to be the major source of nutrition across all areas and sampling periods. In January, the secondary prey of burbots in the Huma reach of the upper Amur River was aquatic insect larvae, while, in the Tongjiang and Fuyuan reaches of the middle Amur River, the secondary prey was shrimp. The mean stomach fullness index and rate of empty stomachs differed with the sampling area, with the greatest proportion of empty stomachs observed in the Luobei reach of the middle Amur River, and the lowest in the Tongjiang and Fuyuan reaches. The mean stomach fullness index showed the opposite trend. In the Huma reach, the contributions of fish to the diet and the mean stomach fullness index were significantly higher in May than in October and January. The study provides the first detailed information on the population age and sex structure, growth patterns, and feeding ecology of burbots from the Amur River, China. The results will aid in formulating management strategies and regulations for local populations of burbots in the Amur River, China.

1. Introduction

The burbot, Lota lota, is one of only two freshwater fishes with a circumpolar distribution, and it exhibits a wide Holarctic distribution throughout Europe, Asia, and North America. It is also the only freshwater species of the family Lotidae [1,2,3]. In China, burbots are distributed in the northeastern and northwestern parts, including the Amur, Yalu, and Eerqisi Rivers. The Yalu River contains the most southern distribution of the species recorded in Asia [4]. The burbot inhabits cool and cold waters. It spawns in winter at temperatures close to 0 °C and exhibits high fecundity [5,6]. For instance, the individual burbot fecundity in the lower reach of the Ob River in 1996–2007 varied between 0.3 and 3.4 million (mln) eggs, averaging just over 1 mln [7]. The burbot is an opportunistic piscivore [8,9,10]; burbot larvae are pelagic [7,11], and adults are benthic predators [12].

The burbot is commercially fished in China, predominately in winter [13], but it is rarely found in the main stream of the Amur River in summer [14]. In recent years, burbot populations have declined worldwide, with some having been extirpated [2]. The reasons for the reduction vary in different parts of the world; the primary causes appear to be pollution, habitat changes, the effects of dams, and overfishing [2,15,16]. Ten years ago, burbot were on the decline in China [15,17,18], but, according to the latest findings, they have shown a trend of recovery over the past 10 years. Within the Russian part of the Amur River catchment, burbots show a stable abundance, and their resources are underexploited [19]. In the upper Wusulijiang River, a tributary of the Amur River, the weights of the individual burbots fished mostly ranged from 1.0 to 2.5 kg in 2003 [18]. The highest individual size and mass of burbot registered near the Elabuga settlement in 2009–2010 were 56 cm and 1.6 kg, respectively [20]. In the middle of the 20th century, the sizes of burbots in the lower part of the Amur River reached 75 cm [14].

The population structure, growth, and diet of burbots have long been studied in Europe, Siberia, and North America [21,22,23,24,25,26,27]. Data on burbots from the Russian part of the Amur River basin have also been published in a few papers [14,20,28,29]. No data are available for the Amur River in Northeast China. The goals of the present study were to (1) analyze the age and sex composition of the burbots inhabiting the Amur River in China, (2) calculate their growth characteristics, and (3) explore the burbot’s diet and its regional and seasonal variation. The study aimed to fill the existing gap in the knowledge of burbot biology. The results will provide information essential for the local protection and management of the species.

2. Materials and Methods

2.1. Sampling Area

The upper and middle stretches of the Amur River follow the boundary between China and Russia. The Amur River remains frozen from November through April (~171 days), with the ice thickness ranging from 0.9 to 1.5 m. Its unique ecosystem, topography, and climate provide a habitat for 96 fish species, many cold-water-adapted, including salmonids, whitefish, graylings, and burbots [30]. The present study examined four sampling areas of the Amur River (47°40′ to 51°58′ N, and 127°27′ to 134°31′ E), including the upper Huma reach and the middle Luobei, Tongjiang, and Fuyuan reaches (Figure 1).

2.2. Sample Collection

A total of 749 burbot specimens were collected by fishermen using drift gill nets (mesh size: 2 × 2 cm, 3 × 3 cm, 4 × 4 cm, 5 × 5 cm, and 6 × 6 cm) and a fish cage (mesh size: 0.4 × 0.4 cm) in all locations. In the Huma reach, samples were taken in October 2022 (n = 63), January 2023 (n = 91), and May 2023 (n = 153). In the Luobei, Tongjiang, and Fuyuan reaches, samples were taken in January 2023 (n = 168, 63, and 211, respectively). The captured fish were sent to the laboratory in a frozen condition. In the laboratory, the fish were weighed to the nearest 0.1 g, and the body length (standard length) was measured to the nearest 1.0 mm. The fish were dissected for sex determination and gut extraction.

2.3. Population Age Structure

The sagittal otolith of 641 specimens was used to determine age. For consistency, we studied the left otolith and used the right only if the left was missing or broken. The otolith was embedded in epoxy, and both sides were polished using abrasive paper until the growth centre was clearly visible [31].

The treated otolith was viewed under a stereomicroscope with brightfield illumination, first upward and then backward. The pellucida and an opaque zone form an annual ring, and otoliths that had formed one annual ring but not a second ring were put into the 1⁺ age class in this study. The otolith was examined by two readers, and the average between-reader percent error was calculated [32]. If the age class estimate of the two readers differed, a third reader estimated the age of the otolith. The final age class was confirmed when two of the three readers agreed. If there was no consensus among three readers, the otolith was deemed unreadable. A two-sample Kolmogorov–Smirnov test was used to examine differences in the fractional age distribution between sexes (α = 0.05) [33] using SPSS 16.0 (IBM SPSS Inc., Chicago, IL, USA).

2.4. Growth Pattern

The length–weight relationship (LWR) was calculated using the equation W = aL^b [34], where W = the body weight (g), L = the total length (cm), a = the intercept, and b = the slope. The parameters a and b were estimated through the logarithmic transformation log^W = log^a + blog^L.

We calculated the von Bertalanffy growth function (VBGF) [35] to represent growth patterns based on age and length according to the formula

VBGF, l_t = L_∞(1 − e^{−k(t−t₀)}),

where l_t is the predicted body length in mm, L_∞ = the mean asymptotic size, k = the growth coefficient for each year, t = the age in years, and t₀ = the hypothetical age at which the body length equals 0. All the growth parameters were modelled in SPSS 16.0.

2.5. Stomach Content Analysis

The stomachs of the burbots were extracted, labelled, and placed in 10% buffered formalin until processing. In the laboratory, the food items were identified to the lowest possible taxonomic level using a stereomicroscope and relevant standard taxonomic keys [36,37,38]. The items of each identified taxon were counted, and the wet mass of each prey item was measured to the nearest 0.1 mg using an electronic analytical balance. The prey items were categorized into six groups—fish, frogs, aquatic insect larvae, shrimp, mollusks, and phytodetritus—with the aim of reducing the error caused by comparisons among taxonomic levels [39]. The prey composition is expressed as the percentage weights (W%), numerical percentages (N%), and percentage frequencies of the occurrence (F%) of prey items [40]. The index of relative importance (IRI) [41] was analyzed using the formula IRI = (W% + N%) ∗ F%.

We used the Kruskal–Wallis nonparametric rank test to identify spatial and seasonal differences in the mean stomach fullness index (IF) using the formula IF = (the weight of the stomach contents/body length) × 100; however, there was a good correlation between the weight of the stomach content of the food mass and the body length of the fish [42,43]. χ2 tests of independence were used to assess spatial and seasonal differences in the rate of empty stomachs [44] using the formula (the number of empty stomachs/the total number of samples) × 100.

3. Results

3.1. Length, Weight, and Sex Ratio

Of the 749 burbots sampled, 357 were female, 344 were male, and 48 were of undetermined sex. The female/male ratio of 1.04:1 did not significantly differ from 1:1 (χ² = 0.241, p = 0.623). The standard length ranged from 175 to 595 mm, and the weight from 73.5 to 1958.7 g. Males were significantly longer than females (D = 1.646, p < 0.01); the mean standard body lengths of males and females were 382 ± 85 and 363 ± 90 mm, respectively. Weight did not differ significantly between sexes (D = 1.313, p = 0.063). The overall length/weight regression indicated that burbots became progressively slenderer as they increased in length: log₁₀^[weight] = −4.58 + 2.80 ∗ log₁₀^{[body length]} (R² = 0.94) (Figure 2). There was a significant difference between the b value (b = 2.80) and 3 according to a t test (p < 0.05); the results show that the burbot was an allometrically growing fish.

3.2. Age and Sex Composition

After the elimination of missing, damaged, and unreadable otoliths, 641 otoliths were available for age analyses: 283 females, 313 males, and 45 of undetermined sex. The age ranged from 1⁺ to 7⁺ years. Both the male and female fractional ages ranged from 1⁺ to 7⁺ years. There were more females than males in the age class 1⁺ (sex ratio: 1.21:1), and the contributions of the females and males in the age classes 2⁺ and 3⁺ were equal (sex ratios: 0.96:1 and 0.88:1, respectively), as were those in the age classes 4⁺ and 5⁺ (sex ratios: 1.14:1 and 1.13:1, respectively). At 6⁺ and 7⁺ years, a dominance of males was recorded (sex ratios: 0.36:1 and 0.38:1, respectively) (Figure 3). The between-reader average percent error was 10.0% for all the samples.

3.3. Growth

The VBGF was calculated for ages 1⁺ to 7⁺ years; the standard lengths ranged from 205 to 565 mm (352 ± 87 mm), ranging from 221 to 565 mm (347 ± 86) for females and 212 to 565 mm (371 ± 85) for males (Figure 4). The ages sampled using the VBGF produced estimates of L_∞ = 596, K = 0.221, and t₀ = −0.771 (R² = 0.844), and the female sample ages produced estimates of L_∞ = 625, K = 0.208, and t₀ = −0.756 (R² = 0.830), while the male sample ages produced estimates of L_∞ = 584, K = 0.219, and t₀ = −0.98 (R² = 0.869) (Figure 4). There were differences in the growth of burbots in different locations, and the ages sampled in the upper reach using the VBGF produced estimates of L_∞ = 764, K = 0.110, and t₀ = −2.029 (R² = 0.722), while the ages sampled in the middle reach using the VBGF produced estimates of L_∞ = 525, K = 0.384, and t₀ = 0.01 (R² = 0.886) (Figure 4).

3.4. Food Composition

Of the 749 specimens, 685 (91.5%) had food in the stomach, while the stomachs of 64 were empty. Prey items were classified into six groups: fish, frogs, aquatic insect larvae, shrimp, mollusks, and phytodetritus (

Table 1. Food composition of burbots in different seasons in Heilongjiang River, China, 2021–2022.

Prey Group	Sampling Area and Season
	Spring in Huma Reach				Autumn in Huma Reach				Winter in Huma Reach				Winter in Luobei Reach				Winter in Tongjiang Reach				Winter in Fuyuan Reach
	N%	W%	F%	IRI	N%	W%	F%	IRI	N%	W%	F%	IRI	N%	W%	F%	IRI	N%	W%	F%	IRI	N%	W%	F%	IRI
Fish	19.66	77.39	74.50	7229.57	54.09	89.82	75.86	10,916.67	16.30	91.16	31.87	3424.57	68.42	89.23	48.80	7693.54	69.17	94.50	95.24	15,587.50	54.94	92.21	86.47	12,724.11
Cyprinidae	4.38	36.64	20.13	825.83	27.24	45.75	25.86	1887.56	2.59	31.21	4.40	148.57	3.76	19.23	4.00	91.96	25.76	43.95	39.68	2766.47	17.93	49.30	35.27	2370.59
Sarcocheilichthys czerskii	0.11	0.75	0.67	0.58	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—
Carassius auratus	0.21	3.36	1.34	4.80	—	—	—	—	—	—	—	—	—	—	—	—	1.22	3.04	7.94	33.82	0.08	0.88	0.48	0.47
Opsariichthys uncirostris	0.11	0.20	0.67	0.20	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	0.41	3.35	2.42	9.09
Pseudolaubuca engraulis	0.11	2.41	0.67	1.69	—	—	—	—	1.11	10.35	1.10	12.60	—	—	—	—	4.67	10.87	12.70	197.27	2.24	8.20	6.28	65.57
Hemiculter leucisculus	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	0.33	2.69	1.45	4.39
Hemibarbus maculatus	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	0.20	0.41	1.59	0.97	—	—	—	—
Xenocypris argentea	0.96	9.81	4.03	43.39	—	—	—	—	—	—	—	—	0.75	4.28	0.80	4.02	1.01	2.03	3.17	9.66	2.41	5.95	5.31	44.43
Pseudorasbora parva	—	—	—	—	2.72	6.51	6.90	63.68	—	—	—	—	—	—	—	—	—	—	—	—	0.17	0.37	0.97	0.52
Rhodeus sericeus	—	—	—	—	1.95	1.71	6.90	25.22	—	—	—	—	—	—	—	—	0.41	0.18	3.17	1.87	0.50	0.39	2.42	2.15
Acheilognathus macropterus	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	0.81	3.86	6.35	29.64	0.33	1.41	1.93	3.37
Rhynchocypris lagowskii	—	—	—	—	4.28	8.44	5.17	65.77	0.37	4.38	1.10	5.22	—	—	—	—	—	—	—	—	—	—	—	—
Phoxinus phoxinus	—	—	—	—	2.72	1.77	3.45	15.48	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—
Ladislavia taczanowskii	0.11	0.71	0.67	0.55	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	0.08	0.03	0.48	0.05
Squalidus argentatus	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	1.62	0.94	1.59	4.07	0.25	0.34	0.48	0.28
Gnathopogon mantschuricus	0.11	0.33	0.67	0.29	3.50	8.94	8.62	107.22	—	—	—	—	—	—	—	—	—	—	—	—	0.17	0.62	0.97	0.76
Leuciscus waleckii	0.11	2.07	0.67	1.46	—	—	—	—	—	—	—	—	0.75	0.13	0.80	0.71	—	—	—	—	—	—	—	—
Gobio cynocephalus	0.11	0.88	0.67	0.66	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—
Culter alburnus	0.11	1.15	0.67	0.84	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—
Unknown fish	2.35	14.96	12.08	209.16	12.06	18.39	10.34	315.00	1.11	16.47	3.30	57.96	2.26	14.82	2.40	40.99	15.62	22.22	20.63	780.77	10.95	25.06	19.81	713.38
Cobitidae	0.53	1.18	3.36	5.75	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—
Lefua costata	0.11	0.37	0.67	0.32	0.78	5.22	3.45	20.69	0.74	8.05	2.20	19.32	—	—	—	—	—	—	—	—	—	—	—	—
Cobitis	0.43	0.81	2.68	3.33	—	—	—	—	—	—	—	—	0.75	2.59	0.80	2.67	—	—	—	—	0.08	0.05	0.48	0.06
Siluridae	—	—	—	—	0.78	0.01	3.45	2.72	—	—	—	—	—	—	—	—	—	—	—	—	0.08	0.37	0.48	0.22
Silurus asotus	—	—	—	—	0.78	0.01	3.45	2.72	—	—	—	—	—	—	—	—	—	—	—	—	0.08	0.37	0.48	0.22
Cottidae	—	—	—	—	—	—	—	—	0.37	3.29	1.10	4.02	—	—	—	—	—	—	—	—	0.08	0.07	0.48	0.08
Unknown fish	—	—	—	—	—	—	—	—	0.37	3.29	1.10	4.02	—	—	—	—	—	—	—	—	0.08	0.07	0.48	0.08
Cyclostomata	0.75	1.85	4.70	12.20	0.78	1.28	1.72	3.55	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—
Lampetra reissneri	0.75	1.85	4.70	12.20	0.78	1.28	1.72	3.55	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—
Unknown fish	14.00	37.72	56.38	2915.68	24.51	37.55	53.45	3317.26	12.59	48.62	26.37	1614.51	63.91	67.41	45.60	5988.34	43.41	50.55	77.78	7307.51	36.76	42.41	70.05	5546.31
Aquatic insect larvae	78.42	20.99	72.48	7205.50	42.41	4.30	34.48	1610.78	81.85	7.38	34.07	3039.85	1.50	0.00	1.60	2.41	0.20	0.07	1.59	0.44	0.41	0.03	2.42	1.07
Odonata	19.44	10.58	44.97	1350.03	5.06	3.22	10.34	85.62	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—
Siebolduis albardae	3.74	2.15	11.41	67.18	3.50	1.99	5.17	28.38	0.37	0.11	1.10	0.52	—	—	—	—	—	—	—	—	—	—	—	—
Gomphidae	8.12	4.65	21.48	274.26	0.78	0.41	3.45	4.11	—	—	—	—	—	—	—	—	0.20	0.07	1.59	0.44	0.08	0.02	0.48	0.05
Unknown larvae	7.59	3.78	21.48	244.09	0.78	0.82	1.72	2.76	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—
Trichoptera	45.09	7.17	11.41	596.17	—	—	—	—	0.74	0.14	2.20	1.94	—	—	—	—	—	—	—	—	—	—	—	—
Hydropsychidae	45.09	7.17	11.41	596.17	—	—	—	—	0.37	0.07	1.10	0.49	—	—	—	—	—	—	—	—	—	—	—	—
Stenopsychidae	—	—	—	—	—	—	—	—	0.37	0.07	1.10	0.48	—	—	—	—	—	—	—	—	—	—	—	—
Megaloptera	0.75	0.06	2.68	2.18	0.78	0.05	3.45	2.86	1.11	0.02	3.30	3.72	0.75	0.00	0.80	0.60	—	—	—	—	—	—	—	—
Sialidae	0.75	0.06	2.68	2.18	0.78	0.05	3.45	2.86	1.11	0.02	3.30	3.72	0.75	0.00	0.80	0.60	—	—	—	—	—	—	—	—
Plecoptera	11.54	2.91	29.53	426.60	33.85	1.51	18.97	670.70	77.41	6.69	28.57	2402.72	—	—	—	—	—	—	—	—	0.33	0.01	1.93	0.65
Pteronarcyidae	1.71	1.03	6.71	18.38	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—
Unknown larvae	9.83	1.88	22.82	267.17	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	0.17	0.00	0.97	0.16
Ehemeroptera					0.78	0.01	1.72	1.36					—	—	—	—	—	—	—	—	—	—	—	—
Hemiptera	0.43	0.06	2.01	0.98	1.17	0.15	1.72	2.27	1.11	0.19	2.20	2.87	—	—	—	—	—	—	—	—	0.17	0.00	0.97	0.16
Unknown larvae	0.43	0.06	2.01	0.98	1.17	0.15	1.72	2.27	1.11	0.19	2.20	2.87	—	—	—	—	—	—	—	—	0.17	0.00	0.97	0.16
Unknown aquatic insect larvae	1.18	0.21	6.71	9.32	0.78	0.18	3.45	3.30	1.11	0.24	3.30	4.44	0.75	0.00	0.80	0.60	—	—	—	—	—	—	—	—
Shrimp	—	—	—	—	—	—	—	—	—	—	—	—	17.29	2.48	8.80	174.01	28.60	5.15	50.79	1714.27	42.16	7.36	52.66	2607.36
Palaemonetes sinensis	—	—	—	—	0.39	0.60	1.72	1.71	—	—	—	—	—	—	—	—	—	—	—	—
Exopalaemon modestus	—	—	—	—	—	—	—	—	—	—	—	—	10.53	1.79	4.00	49.27	26.57	4.44	41.27	1279.91	33.61	6.40	32.85	1314.29
Unknown	—	—	—	—	—	—	—	—	—	—	—	—	6.77	0.69	4.80	35.80	2.03	0.71	11.11	30.41	8.55	0.96	19.81	188.31
Mollusks	—	—	—	—	—	—	—	—	—	—	—	—	0.75	0.11	0.80	0.69	—	—	—	—	—	—	—	—
Gastropoda	—	—	—	—	—	—	—	—	—	—	—	—	0.75	0.11	0.80	0.69	—	—	—	—	—	—	—	—
Frogs	0.11	0.54	0.67	0.43	0.39	3.10	1.72	6.02	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—
Rana amurensis	0.11	0.54	0.67	0.43	0.39	3.10	1.72	6.02	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—	—
Phytodetritus	1.82	1.09	10.74	31.17	2.72	2.18	10.34	50.74	1.85	1.45	5.49	18.16	12.03	8.18	12.00	242.47	2.03	0.28	14.29	32.92	2.49	0.41	13.53	39.16

). Fish represented the most important prey group. Both the W% and F% for fish were high, and its IRI value was the highest among all the prey items, with cyprinids being the most important prey in all the sampling areas and seasons. Secondary prey included aquatic insect larvae and shrimp, with larvae found in all the sampling areas and seasons. Frogs and mollusks were observed in the burbots’ guts randomly. Phytodetritus was found in all the sampling areas and seasons, with a low IRI, and may have been incidentally consumed during feeding on other organisms.

3.5. Regional Variation in Diet

To ensure a sufficient number of samples, the burbot diet was analyzed with respect to regional differences from the January sampling, which included all locations. Both the percentage of empty stomachs (χ² test, χ² = 24.70, and p < 0.001) and the mean ± standard error (S.E.) stomach fullness index (Kruskal–Wallis test, Hc = 201.18, and p < 0.001) showed significant differences among the groups (Figure 5). The percentage of burbots with empty stomachs was the highest in the Luobei reach and lowest in the Tongjiang reach (Figure 5). The mean stomach fullness was the highest in the Tongjiang reach and lowest in the Luobei reach (Figure 5).

Since frogs are not found in the winter, the prey categories consisted of fish, aquatic insect larvae, shrimp, mollusks, and phytodetritus (Table 1). The N% and F% values of fish in the stomach were lower than those of aquatic insect larvae in the Huma reach, but the opposite was true in the Luobei, Tongjiang, and Fuyuan reaches. Aquatic insect larvae were the main prey only in the Huma reach; the frequency of occurrence and numerical percentage in the other reaches were <3%. The stomachs of burbots in the Luobei reach occasionally contained shrimp, but this was more prevalent in the Tongjiang and Fuyuan regions, with frequencies of occurrence > 50% in these two reaches. Mollusks were found only in the Luobei reach. The diet composition in the four river stretches showed no significant differences with respect to primary prey items but differed in terms of secondary prey.

3.6. Seasonal Variation in Diet

In order to ensure a sufficient number of samples, the burbot diet was analyzed with respect to season only in the Huma reach. Since shrimp and mollusks were not observed in the stomachs of burbots in the Huma reach, prey items were classified into four groups: fish, aquatic insect larvae, frogs, and phytodetritus (Table 1). The mean stomach fullness index (Kruskal–Wallis test, Hc = 50.78, and p < 0.001) showed significant differences among seasons but the percentage of empty stomachs (χ² test, χ² = 3.00, and p > 0.05) did not significantly differ. The mean stomach fullness was the highest in May and lowest in January (Figure 5). The importance of fish and aquatic insect larvae as prey was similar in May and January, but the IRI of fish was higher than that of aquatic insect larvae in October (Table 1). Frogs were not found in the stomachs of burbots in January.

4. Discussion

The study showed that the maximum age of the burbots collected was 7⁺ years, their maximum body length was 595 mm, and their maximum weight was 1958.7 g in the Amur River. This corresponds to the results for burbots from the Elabuga settlement located 150 km downstream of the Amur River [20]. In the upper reaches of the Mudanjiang River, the maximum age of the burbots was 6 years, the maximum body length was 589 mm, and the maximum weight was 1800 g [45]. In the upper reaches of the Eerqisi River, the maximum age of the burbots was 5 years, the maximum body length was 570 mm, and the maximum weight was 1408 g [46]. This is lower than the recorded values of the maximum age of the burbots in the northern part of their distribution range. Thus, the oldest burbot individuals from the Ob River are aged 21+, with the most common age classes being 4+–13+ for males and 5+–15+ for females [7,47]. Moreover, maximal life longevities of 24+ and 25+ were documented for burbots from the Enisey River and Indigirka River, respectively [48,49]. Our results for the age structure are close to the published data for the lower reaches of the Volga River and Danube River [50,51]. They correspond to the known phenomenon of an increase in the life longevity of most fish species when we move from southern to northern populations [52].

According to the standard proposed by Branstetter [53], K values of 0.1–0.2 per year indicate medium-growth fish, and those of 0.20–0.50 per year indicate fast-growing fish. In the Amur River, the K value of burbots was 0.221, so they can be considered fast-growing fish. However, the growth of burbots varies across space; they were medium-growth fish (K = 0.110) in the upper reach of the Amur River and fast-growing fish (K = 0.384) in the middle reach. This finding corresponds to the results of burbot studies conducted in the Ob–Irtysh basin [47]. Fish from the upper reaches of the catchment representing resident life histories experience a lower availability of forage resources compared to burbots from the lower reaches representing migrating individuals. The differences in the life strategies and environment were reflected in the differences in the diet, growth rate, and parasitofauna of the burbots from different parts of the Ob–Irtysh basin [47]. According to historical reports, the average biomass of benthic animals in the middle reaches of the Amur River was 34.62 g/m², and the average biomass in the upper reaches was 20.6 g/m² [54,55]. Our investigation found that fish production in the middle reaches of the Amur River is higher than in the upper reaches. The reduced growth of fish from the upper reach of the Amur River revealed in this study may be explained by the reduced abundance of food resources, leading to a higher stomach fullness index for burbots in the middle reach (Tongjiang reach and Fuyuan reach) compared to the upper reach (Huma reach). Pauly [56] believes that the growth rate of fish is negatively related to the water temperature. This is true for most fish species but not for burbots. The burbot is an exceptionally cold-water-adapted species adapted to living under ice conditions [6]. With a decrease in the temperature of the water, the enzymatic digestion of food in the burbot’s stomach increases, and vice versa [57]. In the case of high water temperatures, even if forage organisms are available, the burbots eat less and the digestion of food slows down [58]. The upper reach of the Amur River had a higher latitude and a lower temperature, so this is unlikely to be the reason for the slowing growth of the burbots in the upper reaches. In addition to food resources, light and other environmental factors affect the individual growth of fish [59]. An increase in light intensity negatively affects burbot growth in the adult stage but positively influences the growth of larvae and early fry during the first few months after hatching [7,60].

The contributions of the female and male burbots were different across age classes, and the males were dominant at ages 6+ and 7+, leading to the difference in the average sizes of fish of different sex. The same was observed for burbots from the Elabuga site. No females were observed among the oldest individuals aged 7+ [20]. Based on the sex ratio of mature burbots in the upper reaches of the Mudan River [45], most burbots reached sexual maturity at four years, with males outnumbering females after this time, similar to our findings. The female/male ratio (0.9:1) of all the burbots (juvenile and sexually mature fish) in this study was greater than the ratio (0.65:1) of sexually mature burbots (at least 4 years old), perhaps because of male migration to spawning areas [25]. Our findings on the sex ratio are typical for resident burbots in the Ob–Irtysh basin, with a sex ratio close to 1:1. Among the migratory form of the species from the lower reach of the Ob River catchment during the upward spawning migration, the ratio of females to males varied from 1:2 to 1:4. During the downward post-spawning migration, females usually predominate [7].

Burbots in the Amur River were found to be carnivorous, primarily feeding on fish and secondarily on aquatic insect larvae and shrimp. In the upper reaches of the Mudan River, burbots older than 1+ mainly feed on fish [45], and this was the minimum age of the burbot specimens analyzed in the current study. Burbots in the waters of the Irtysh River in Northwest China are also chiefly piscivorous [46,61]. In the Amur River, we see the importance of fish and secondary prey as prey differed from the sampled area, with the IRI value of fish being the lowest in the Huma reach. The contribution of aquatic insect larvae to the burbot diet was greater than in the Huma reach than in other areas, while shrimp were more common in the diets of burbot from the Tongjiang and Fuyuan populations. This phenomenon may be related to the distribution and abundance of prey species, as seen in other fish species [62,63]. Our unpublished data show that the fish resources in the Huma reach were the lowest among the sampling areas. Additionally, there are no reports of Palaemonetes sinensis or Exopalaemon modestus shrimp occurring in the Huma reach, but they are abundant in the Luobei, Tongjiang, and Fuyuan reaches [54,55,64,65]; this explains why shrimp were not found to be consumed in Huma but were consumed in other sampled areas. In the upper parts of the catchment, the ecosystem productivity is low, especially in winter, and the food resources are unable to maintain a large number of predators. This leads to a shift in the burbot diet towards an increase in invertebrate consumption and a decrease in stomach fullness [47]. Similarly, in other areas such as the Elabuga site, shrimp were also an important secondary prey for burbot, with fish being the primary type of prey [20]. There were significant regional differences in the mean stomach fullness index and rate of empty stomachs; the rate of empty stomachs was the highest in Luobei and lower in Tongjiang and Fuyuan, while the stomach fullness index showed the opposite pattern. A higher fish biomass is observed in Tongjiang and Fuyuan (unpublished data), and there are more opportunities for burbots to prey on fish. The mean stomach fullness index was the highest in the Tongjiang reach, and the rate of empty stomachs was the lowest. The Tongjiang reach is located at the confluence of the Amur River and its largest tributary, the Songhua River, which is an area of abundant prey. The low filling index and high frequency of empty stomachs in Luobei could be attributed to both the low density of prey and the increased number of burbot breeders in limited spawning areas. A similar situation is known for spawning burbot individuals in the Ob Basin in winter [7,66]. The Mudan River is a secondary tributary of the Amur River; in the upper reaches of the Mudan River, the burbot reproductive migration period is November to March, and the peak spawning period is January, with the cessation of feeding shortly before spawning [45]. This may account for the low mean stomach fullness index and high rate of empty stomachs observed in winter in this study. In late March, the burbots complete their reproductive migration from Jingpo Lake to the upper reach of the Mudan River and enter a fattening phase [67], likely explaining the high stomach fullness index and low empty stomach rates in May. The choice of prey is also related to the energy contained in the prey [68]. According to the “optimal feeding theory”, the predator will attempt to obtain large prey with a nutrient content to compensate for the energy expended in predation [69]. The burbots sampled in October in the Huma reach of the Amur River preferred fish, possibly in order to replenish the energy lost through reproduction and migration at the population level.

5. Conclusions

This study provides information on the age and sex structure, growth, and seasonal and regional variation in the diet of burbots (Lota lota) in the Amur River, Northeast China. The age of the burbots ranged from 1+ to 7+ years, and allometric growth was observed. The von Bertalanffy growth equation (L_t = 596 [1 − e^{−0.221 (t + 0.771)}) indicated an estimated asymptotic length (L_∞) of 596 mm and a fast growth rate (k = 0.221), and the growth showed regional variation. Burbots were found to be carnivorous, and fish were their main prey; both the secondary prey and feeding intensity differed regionally. To ensure the sustainability of this species, several strategies could be implemented, such as the regular monitoring of population dynamics and prey fish, size restrictions for fishing, and regulated fishing seasons. These actions could significantly impact the protection and management of burbots in the Amur River.