Seasonal Dynamics of Feeding Habits of a Cyprinid Fish, Saurogobio dabryi in the Downstream of the Jialing River, China

J. Ma1, F.B. Zhang1,2, J. Li1, Z.Y. Lv1, C. Zhang1, L. Mao1 and Y. Zeng1*

1College of Life Science, Southwest Branch of the National Freshwater Fishery Engineering Technology Research Center, China West Normal University, Nanchong 637000, China

2College of Environmental Science and Engineering, China West Normal University, Nanchong 637009, China

ABSTRACT

This research studied the food composition and feeding rhythm of Saurogobio dabryi in the lower reaches of the Jialing River, aimed to explore the seasonal difference of its feeding habits. Gut contents of 268 S. dabryi in the downstream (Hechuan section) of the Jialing River were collected seasonally from September 2015 to August 2016. The feeding habits of S. dabryi were studied by microscopic examination, analysis of similarity, and the Amundsen graphical method. A total of 26 food categories were identified, among which algae and organic detritus were the dominant food source for S. dabryi. Animal prey contributed relatively low proportions to the food of S. dabryi. Seasonal variations of food composition of S. dabryi were significant (P<0.05). Hierarchical cluster analysis shows that the food composition in autumn was significantly different from other seasons at a similarity level of 60%. The results indicated that the feeding rhythm of the S. dairyi in the lower reaches of the Jialing River showed significant seasonal changes (P<0.05); The feeding intensity and food amount gradually increased from spring to winter, which may be related to the morphological structure, breeding period, special habitat, and seasonal changes of biological prey of S. dabryi.

Article Information

Received 19 January 2022

Revised 05 February 2022

Accepted 27 February 2022

Available online 28 July 2022

(early access)

Published 28 July 2023

Authors’ Contribution

JM, FBZ, JL and YZ contributed to

the initial design of this project. MJ, LM, ZYL and CZ collected animals samples. JM and CZ conducted the experiments, bioinformatics analyses and prepared the manuscript.

Key words

Saurogobio dabryi, Feeding habits, Seasonal variation, Feeding rhythm, Jialing River

DOI: https://dx.doi.org/10.17582/journal.pjz/20220119100124

* Corresponding author: [email protected]

0030-9923/2023/0005-2131 $ 9.00/0

Copyright 2023 by the authors. Licensee Zoological Society of Pakistan.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

Introduction

Fish show a variety of adaptation mechanisms in response to changing environments. They not only passively accept the environment but also actively adapt to the environment (Foote et al., 1992). In recent years, an increasing amount of studies have shown many fish have corresponding alterations on growth, reproduction, and especially feeding activities to the great changes in the aquatic ecological environment (e.g., building dams, sewage discharge) (Hahn, 2007; Ferrareze et al., 2014). Fish will adopt different feeding strategies to actively adapt to changes in the environment, such as increasing feeding time, expanding predation types, reducing feeding intensity, and competing for interspecific alternate feeding to maintain the continuity of the population under the changed environmental pressure (Oliveira et al., 2018; Rayner et al., 2009). Therefore, studying the feeding habits of fish and their dynamic changes are of great significance for understanding fish’s adaptation mechanisms to the environment and formulating fish protection and management plans (Done, 1999).

The study on the fish diet is based on the composition of the gut contents and the importance of food. The commonly used methods include the frequency of occurrence method, numerical method, gravity method, and the index of the relative importance (Hyslop, 1980). Prejis and Prejis (1987) discovered that the prey items of Tetragonopterus argenteus were mainly composed of crustaceans, chironomid larvae, and coleoptera through the gravimetric method, and explored the relationship between its special geographical environment and seasonal changes in prey organisms by gravity method. Grabowska et al. (2010) adopts a variety of methods such as the frequency method and relative importance index to study the dietary sources of racer goby (Neogobius fluviatilis). The results showed that there was no obvious difference in the food composition of chironomid larvae, small mollusks, and crustaceans, which may be related to its wide predation range and opportunistic predation strategy as an invasive species.

Saurogobio dabryi (Cyprinidae: Gobioninae), commonly known as boat nail, likes flowing water life. It is not only an important river fish but also one of the main economic fish in the Jialing River (Zhang et al., 2018). In recent years, the original aquatic ecological environment has undergone a great change because of the construction of cascade hydropower projects on the Jialing River, which has caused adverse effects on fish who like rapids or flowing water (Zeng, 2012). However, detailed feeding research on the rapids or flowing water living fish in the Jialing River cascade hydropower project water areas were scarce. It is not known whether its food habits will change with the seasons under the new environment (slow water conditions) or not. This study selected S. dabryi as an example of rapids or flowing water fishes in the lower reach of the Jialing River, to explore its food composition, feeding rhythm, and to analyze the seasonal differences of their feeding habits, using combined methods of microscopic examination, analysis of similarity, and the Amundsen graphical method. The result will provide a reference for the protection and management of fish resources in the Jialing River.

MATERIALS AND METHODS

Sample collection and prey analysis

The sampling site was located at the Hechuan River section of the lower Jialing River (29°30′-29°40′N, 106°30′-106°40′E), within a range of about five kilometers (Fig. 1). The sampling point has a straight river section with abundant fish resources (Jiang and He, 2008). Sampling was performed monthly from September 2015 to August 2016, using gillnet (mesh size 30 mm), cast net (mesh size 30 mm), and ground cage (mesh size 15 mm). Water temperature, PH, and other indicators (e.g., dissolved oxygen, nitrogen, and phosphorus content) of the sampling site were measured and recorded. In the field experiment, the standard length (SL, 1 mm) and body weight (BW, 0.01 g) were measured immediately after capture (Zhang et al., 2018). To prevent prey from being digested, the gut contents were fixed instantly after capture in a 4% formaldehyde solution for further analysis. The gut was divided into three parts: foregut, midgut, and hindgut according to gut morphology. The degree of filling of different gut segments was divided into six grades, which indicated that food accounted for about 0%, 25%, 50%, 75%, 100% of gut volume, and gut expansion (Yin, 1993).

To reduce the error caused by digestion, only samples with gut fullness degree ≥ 2 were selected for the diet analysis. The food prey was identified and counted by a dissecting microscope and a binocular microscope, then its weight was calculated through the length-weight relationship (±0.0001 g) (Baumgärtner And Rothhaupt, 2003). Even small fragments must be identified very carefully to minimize the underestimation of small and soft prey. During identification, two pieces were generally counted and the average value was used, aquatic insects were generally identified to the family or genera level, and algae were usually identified to the genera level (Bernal et al., 2015; Didenko et al., 2018).

 

Data analysis

To evaluate whether the number of samples used for diet analysis was sufficient, non-empty cumulative prey curves were constructed by Estimate S 9.1.0 (http://purl.oclc.org/estimates) software (Espinoza et al., 2013). The slope of linear regression (b) of the last five subsamples was used for evaluation, where b ≤ 0.5 indicated that samples were enough for diet description (Brown et al., 2012).

This research used frequency of occurrence (% F), percentage number (% N), weight percentage (% W), index of the relative importance (IRI), and percent index of relative importance (% IRI) (Hyslop, 1980) to quantitatively evaluate the importance of prey, the specific calculation method was as follows: % F= (the number of guts containing one prey item / the total number of non-empty guts) × 100. % N= (the number of one prey item / the total number of prey items) × 100. % W= (the weight of guts containing one prey item/ the total weight of prey items) × 100. IRI= (% N + % W) ×% F. % IRI= (index of the relative importance of one prey item / index of the relative importance of the total prey items) × 100.

The study test seasonal differences in the feeding habits of S. dabryi by Analysis of Similarity (ANOSIM) (Clarke and Warwick, 2001), which was based on the Bray-Curtis similarity index. The % W index was selected because the index can overcome the problems that digestion poses for enumerating prey items (White et al., 2004). In the analysis, the R statistic was used to measure the similarity of food between different seasons. At the same time, the Hierarchical cluster analysis (UPGMA) method was used to cluster analysis of food composition in different seasons.

Because the use of the gut fullness index cannot accurately reflect the feeding rhythm of fish in the natural state (Devlaming et al., 1982; Cortés, 1997). the empty gut rate and the gut fullness index were used at the same time when studying the feeding rhythm of S. dabryi.

The empty gut rate (%) = (empty gut number/ total number of fish) ×100

The gut fullness index (K) = (gut content weight/ body weight) ×104

The empty gut rate showed a non-normal distribution (Shapiro-Wilks test, P < 0.05). Therefore, the seasonal difference of the empty gut rate was analyzed by the chi-square test (χ2), the seasonal difference of the gut fullness index was tested by analysis of variance.

Using Amundsen’s graphical method (Amundsen et al., 2010) improved on Costello (1990), the frequency of occurrence and prey-specific abundance constitute a two-dimensional graph on the horizontal and vertical coordinates respectively. The distribution of the position of the scattered points to describe the feeding strategy of S. dabryi in the lower reaches of the Jialing River. The formula for calculating the Prey-specific abundance was as follows:

Prey-specific abundance (Pi) = (ΣSi/ΣSii) × 100

Pi was the Prey-specific abundance; Si was the weight of prey i in the gut, Sii was the content weight of the stomach (gut) of the individual with prey i in the gut.

Results

A total of 268 individuals (137 females and 131 males) of S. dabryi were collected and examined, with the SL ranging from 70.5 to 184.0 (112.3 ± 16.7, mean ± SD) mm, and the BW ranging from 3.7 to 44.4 (16.3 ± 6.8) g (Table I). There were also significant differences in the number of samples collected in different seasons, with less in spring and winter, and more in summer and autumn.

Seasonal feeding intensity

The results of the chi-square test indicated that the empty gut rate changed significantly in different seasons (χ2 = 24.24, P < 0.05). The empty gut of S. dabryi was the highest in spring (53.33 %) and the lowest in winter (8.47 %) (Fig. 2). The results of ANOVA showed that there were significant differences in the fullness index among different seasons (F = 7.25, P < 0.05), the highest in winter (62.02 %), followed by autumn (54.40 %) and summer (47.07 %), and the lowest in spring (26.64 %). Besides, S. dabryi showed feeding activities throughout the year, during which its feeding activities were weakest in spring and the strongest in winter.

 

Cumulative curves

The analysis of the prey accumulation curve showed that the curve had reached an asymptote (b < 0.5). Therefore, the number of samples in each season was considered sufficient to describe the diet (Fig. 3).

 

Table I. Sampling of S. dabryi in the lower reaches of the Jialing River in different seasons.

Season	Specimens	Body length (mm)		Body weight (g)
		Range	Mean±SD	Range	Mean±SD
Spring	30(14)	86.0~124.6	103.9±8.0	9.1~25.7	14.9±3.8
Summer	89(69)	70.5~136.0	105.6±16.8	3.7~31.1	14.7±7.1
Autumn	90(73)	86.0~184.0	120.6±18.4	4.9~44.4	17.9±7.9
Winter	59(54)	101.1~147.0	114.3±9.6	11.1~40.5	17.1±5.4
Total	268(210)	70.5~184.0	112.3±16.7	3.7~44.4	16.3±6.8

 

Notes: the parenthesis indicates the non-empty gut sample size.

 

 

Food composition and seasonal variation

The gut content of S. dabryi contained a wide variety of algae, plants and animal prey. A total of 26 different food taxa belonging to 10 main prey categories (e.g., Cyanophyta, Bacillariophyta, Chlorophyta, organic detritus, aquatic insects) were identified (Table II). Among them, organic detritus (% IRI = 28.15), Anabaena (% IRI = 16.92), and Cocconeis (% IRI = 16.74) were the most important food sources for S. dabryi. Although there were many kinds of animal items, the overall proportion was low (% IRI = 1.15).

 

Analysis of similarity (ANOSIM) (Fig. 4) indicated that there was a significant seasonal difference in the food composition of S. dabryi (R= 0.18, P < 0.05). The hierarchical cluster analysis shows that the food composition of S. dabryi in autumn was significantly different from other seasons at a similarity level of 60 % (Bray-Curtis Similarity). Among them, spring was the season with the largest consumption of animal feed (% IRI = 7.79) (Table II), and the contribution rate of organic detritus to the food of S. dabryi was also relatively high (%IRI=31.81). In summer, S. dabryi almost only consumes algae prey (% IRI = 89.41), and the organic detritus was the least in all seasons (% IRI = 10.01). In autumn, it mainly fed on algae (% IRI = 75.22) and organic debris (% IRI = 24.41). In winter, organic debris (% IRI = 40.85) contributes the most to the food of S. dabryi, while the intake of animal feed was very small.

 

Feeding strategy

According to the Amundsen graph (Fig. 5) of the feeding strategy of S. dabryi, most of the prey categories were in the lower part of the graph except for a few types of food, which reflected S. dabryi can be considered as a

 

moderate generalist predator, this will greatly preserve the continuation of the species under harsh environmental conditions. Organic debris, diatoms, cyanophytes, and chlorophytes were the main foods, all of which have a high occurrence rate and abundance of prey. However, the aquatic insects, oligochaetes, polychaetes, rotifers, crustaceans, and sarcodina were a low relatively occurrence rate and rare prey, this was consistent with the relatively low contribution rate of animal feed. Besides, the distribution position of prey indicates that the difference in food composition among different individuals of the S. dabryi population was small, and the degree of food overlap was high.

Discussion

Diet composition

The feeding habits of fish was the result of fish adapting to changes in the living environment, the same fish may have completely different feeding habits in different environments (Zander et al., 1999). Grabowska et al. (2009) found that the monkey goby (Neogobius gymnotrachelus) mainly feeds on amphipods and chironomid larvae in the invasion area (the Baltic Sea), which was quite different from the original place (the Lazim Lake) in food composition. This may be due to the lack of food resources in the invasion area, and adapting strategies of the fish, such as competing for interspecific alternate feeding and opportunistic predation to alleviate the survival pressure (Hermoso et al., 2011). This study found that there were many kinds of food items of S. dabryi, including animal and plant prey (mainly plant prey), indicating that S. dabryi was omnivorous and more plant-eating fish, and its food composition contains more organic detritus and benthic items, which were compatible with the benthic life of S. dabryi, with thick upper and lower lips and special morphological structure of feeding organs (Lv et al., 2019). On the other hand, it was also related to the unique habitat of the Jialing River and the abundance of the prey item. The suitable climatic conditions (e.g., water temperature, light.) of the Jialing River were beneficial to the growth and reproduction of algae and provide abundant plants food for S. dabryi (Long et al., 2008). However, the feeding habits of S. dabryi in the Dadu River and Chishui River showed more preference for animal feed, which were quite different from those in the lower reaches of Jialing River (Li, 2016; Wang et al., 2018). This may be due to the position as a dominant species of S. dabryi in the Jialing River, and its gut structure exhibits allometric growth pattern to adapt to different food compositions (e.g., Cladocera, Chironomid.), which was more competitive than other fishes in obtaining high-quality animal prey resources (Zhang et al., 2018).

Dietary variation

The seasonal variation of fish feeding habits was the result of fish adapting to the fluctuation of the surrounding water environment (Jakubaviciute et al., 2017). Generally, most fish have significant seasonal changes in their food habits, while a few fish have no significant seasonal differences (Hanson, 2002). For example, the food composition of walleye pollock (Theragra chalcogramma) was an obvious seasonal variation in Alaska (Adams et al., 2007), On the one hand, it was related to the seasonal decrease of its prey abundance, on the other hand, it was related to its unique living environment. However, there was no significant difference between feeding habits and seasons in the karstic dace (Telestes karsticus) in Croatia, this was determined by the relatively stable living environment and the abundant food supply in the local river (Marčić et al., 2017).

In this study, we found that the feeding of S. dabryi in autumn was significantly different from that in other seasons. The main food sources of the S. dabryi in autumn were plant preys such as Anabaena and organic detritus. This may be related to the seasonal changes in algae food. Spring and autumn are the peak periods of algae reproduction each year. Cyanophyta and Diatoms were the dominant groups in the lower reaches of the river (the amount of bait is abundant), which are easier to be caught by the S. dabryi than other diets (Li, 2017; Zhang et al., 2015). On the other hand, it may be related to the unique habitat of the Jialing River. In summer, the lower reaches of the river enter the flood season, when a large amount of organic matter enters the water body through scouring and gradually sinks to the bottom to become organic debris, large rainfall and fast flow velocity (Zhou et al., 2008). As the water level of the Jialing River decreases in autumn, the flow rate slows down, and the transparency increases, the relatively stable water environment is conducive to the ingestion of organic debris by S. dabry (Deng et al., 2010). Although there were little differences in the feeding habits of the S. dabry in spring, summer, and winter, there were different food preferences among the seasons. S. dabry consumes the most animal food in spring, which may be a huge energy consumption during the breeding period, and animal food can better meet the demand. However, in summer, the S. dabry almost only ingests algae, and the contribution rate of other preys is little, which is because the Jialing River is in the flood period in summer, the water level rises rapidly, and the water body is turbid, which is not conducive to the feeding activities of S. dabry and other bottom fish. Besides, in the winter, the proportion of organic detritus ingested by S. dabry further increased, which was due to the decrease of water temperature, which led to the reduction of algae population and the difficulty of predation. Similar phenomena have also been reported in other fishes. Tamada (2005) found that seasonal changes in the feeding habits of Rhinogobius giurinus and a narrower food space (limited to food near the nest). This phenomenon was related to the water velocity in the habitat and the abundance of prey organisms, especially during the breeding period.

Feeding rhythm

The feeding activities of most fish have significant seasonal changes, which were related to changes in their physiological characteristics or environmental factors (Bolliet et al., 2001). For example, Olaso et al. (2000) found that the feeding rhythm of adult individuals of Pogonophryne marmorata was greatly affected by the breeding season, which gonads develop rapidly during the reproduction period (accounting for more than 25% of the body cavity), which leads to a significant decrease in feeding rhythm. The Bolliet et al. (2001) research indicated that the feeding rhythm of Oncorhynchus mykiss was more affected by the day and night (night eating) in European, this may be related to the abundance and availability of prey in the environment. The results showed that the feeding rhythm of the S. dabryi in the lower reaches of the Jialing River gradually increased from spring to winter, showing significant seasonal variation (P < 0.05), which was closely related to the breeding period. Spring was the peak period for the reproduction of S. dabryi, and the developed gonads will occupy most of the space in the body cavity of the fish, which leads to the phenomenon of reduced feeding activities during the breeding period. However, they reduced the proportion of plant prey and preferred to choose animal prey to meet their nutritional needs during breeding. The feeding activity of S. dabryi was the strongest in winter. There are two reasons for this: firstly, it may be to consume a large amount of food and convert excess energy into fat for energy storage for overwintering. Secondly, it may reserve energy for reproduction in the next spring so that gonads can develop and mature rapidly in the coming year (Yang et al., 2011).

In the long-term evolution of fish, a series of morphological characteristics adapted to their respective living environment and feeding patterns have been formed (Olsson and Eklov, 2005). This can not only reflect the passive adaptation of fish to changes in the living environment but also better reflect the active choice of their feeding strategy (Delariva et al., 2013). This study investigated the seasonal dynamics of the feeding habits of S. dabryi in the lower reaches of the Jialing River from 2015 to 2016. The results showed that the S. dairyi was omnivorous and partial plant-eating fish, mainly feeding on algae and organic debris. There were significant differences in food composition between autumn and other seasons, the morphology and structure of its feeding organs and the unique habitat of the Jialing River were the main reasons that affect the current food composition of S. dairyi. Besides, there were significant seasonal variations in the feeding rhythm of S. dairyi (P < 0.05). The feeding intensity and feeding amount were the lowest in spring and the highest in winter, which was related to its breeding period and seasonal variation of biological prey.

Acknowledgements

We are grateful to Chen Zhang for his help in sample collection and identification. This research was supported by the National Natural Science Foundation of China (No. 51779210), and the Fundamental Research Funds of China West Normal University (No. 19C007, No. XJJGXH2017122). The authors report no conflicts of interest. The author salone are responsible for the content and writing of the article.

Statement of conflict of interest

The authors have declared no conflict of interest.

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