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Article

The Diversity and Biochemical Composition of Zooplankton as a Potential Indicator of Dietary Requirements for Pikeperch Larvae (Sander lucioperca)

by
Anatoliy Lyutikov
1,*,
Alexander Korolev
1,
Artem Trifonov
1,
Anastasia Zubareva
2 and
Artem Nedoluzhko
3,*
1
Saint Petersburg Branch of “VNIRO”, “GosNIORH” Named After L.S. Berg, St. Petersburg 199053, Russia
2
Institute of Macromolecular Compounds, Branch of Petersburg Nuclear Physics Institute Named by B.P. Konstantinov, National Research Centre Kurchatov Institute, St. Petersburg 199004, Russia
3
Paleogenomics Laboratory, European University at Saint Petersburg, St. Petersburg 191187, Russia
*
Authors to whom correspondence should be addressed.
Hydrobiology 2025, 4(2), 13; https://doi.org/10.3390/hydrobiology4020013
Submission received: 20 February 2025 / Revised: 12 April 2025 / Accepted: 29 April 2025 / Published: 6 May 2025
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Abstract

:
Freshwater fish species play an important role in global aquaculture. Currently, sturgeon, carp, and tilapia are at the forefront of this industry. However, as human populations continue to grow, the demand for new sources of animal protein increases, making the use of other freshwater species in aquaculture essential. The pikeperch (Sander lucioperca) is one of the most promising fish species for European aquaculture, but its usage has been hindered by a lack of effective larval-rearing protocols. Most studies focus on using cultured or nutrient-rich zooplankton for larval cultivation, while natural zooplankton from the local environment are rarely used. In this study, we aim to investigate the nutritional requirements of pikeperch larvae by describing the taxonomic diversity and biochemical composition of zooplankton collected from a natural oligotrophic lake in Northwest Russia. The chemical composition of zooplankton is characterized by a high protein content (up to 70% of dry matter), a moderate lipid content (up to 25%), and a deficiency of certain fatty acids and amino acids. Specifically, there is a low concentration of docosahexaenoic acid and methionine. The dry matter content in the zooplankton averages 10%, with nitrogen-free extracts accounting for 4% and ash making up 4%. These biochemical parameters meet the nutritional requirements of freshwater pikeperch larvae, with the notable exception of the lower levels of DHA and methionine, which are typically characteristic of freshwater zooplankton. This information sheds light on the nutritional requirements of pikeperch larvae and the development of more efficient rearing methods.

1. Introduction

The pikeperch (Sander lucioperca), a species of fish from the Percidae family, has great potential for aquaculture development in Eastern Europe [1,2,3]. However, its low survival rate, cannibalistic behavior, and high incidence of skeletal abnormalities in early development have hindered its introduction into European aquaculture [4,5]. Despite the addition of Artemia nauplii to the diet, the survival of pikeperch larvae remains very low, with an average of only 25% by the 35th day after hatching [6,7].
The poor survival rate of pikeperch larvae during the early stages of development can be attributed to their extremely small size and underdeveloped digestive systems [6,7,8,9,10]. The issues in the development of the larval digestive system may be related to its ineffective enzymatic activities [11,12,13]. This, in turn, limits the ability to produce high-quality artificial feeds for pikeperch larvae. Currently, there are no commercially available feeds specifically designed for these larvae [14].
The development of combined artificial feeds and supplements for pikeperch larvae could reduce labor costs associated with collecting or raising live organisms, as well as reduce the risk of introducing diseases or pollutants [15]. Additionally, the cost of manufactured feeds is likely to be lower than the actual price of Artemia cysts [16].
Numerous attempts have failed to cultivate pikeperch larvae using exogenous nutrition and artificial diets. The survival rate of the larvae in the tests was approximately 0%, with most of them dying within the first two to three weeks [17,18,19,20]. In this regard, modern technology for the industrial rearing of pikeperch relies on feeding larvae with planktonic (mostly zooplanktonic) species only (chlorella, rotifers, Artemia, and copepods) or in combination with artificial supplements. Afterward, pikeperch juveniles are completely transferred to an artificial diet [21,22,23,24,25,26,27,28]. However, cultivated zooplankton often do not meet the nutritional requirements of pikeperch larvae, and various commercial nutrient supplements are used to enrich fish diets in aquaculture [22,29,30]. In particular, cultivated commercial zooplankton often lack polyunsaturated fatty acids [31,32,33], which are essential for the normal growth and development of fish larvae [34].
Thus, most studies on rearing pikeperch larvae use native or nutrient-enriched zooplankton as a starting diet. However, there is evidence that pikeperch larvae fed on natural zooplankton for 28 days have a relatively high survival rate of up to 44% [35]. This is significantly higher than the survival rate of larvae fed a combined diet of zooplankton and Artemia, which is up to 26.7% [6]. It seems that natural zooplankton provide a better nutritional composition for pikeperch larvae.
Unfortunately, studies on the nutrition of early-stage pikeperch larvae are limited, with most focusing on describing species diversity [36,37]. This information is not only of scientific interest but also has practical implications, as it could be used to develop an artificial starter diet for these larvae.
In the present study, we describe the taxon diversity and biochemical composition of natural zooplankton, which constitute a primary food source for pikeperch larvae in the early stages of their development, in a natural lake ecosystem in Northwest Russia (Sukhdolskoye Lake). Herein, we focus on the period from 3 to 21 days post-hatching (dph), as this is when the larvae undergo critical stages of development, such as transition to external nutrition, gas filling of the swim bladder, and complete consumption of fat droplets and the yolk sac (after this period, mortality of the larvae is significantly reduced). We suggest that the biochemical composition of natural zooplankton corresponds to the nutritional requirements for pikeperch larvae, except for a low content of two specific supplements: docosahexaenoic acid (DHA) and methionine. Our findings shed light on the dietary requirements of pikeperch larvae during their early development and suggest that natural zooplankton should not be the only feed source for this species in commercial aquaculture.

2. Materials and Methods

2.1. Pikeperch Larval Rearing Description

The zooplankton probes for this study were collected in 2022 from the oligotrophic Sukhodolskoye Lake (60°36′14.91″ N, 30°23′53.54″ E), the native habitat of pikeperch. The period of zooplankton sampling was synchronized with the development of pikeperch larvae under the conditions of the local fish farm (LLC “Forvat”; https://forvat.ru/, accessed on 23 January 2025), located on the same lake (Figure 1). The sampling period (19 days) corresponded to the time of development of larvae from the beginning of feeding at 3 dph up to 21 dph.
Experimental pikeperch larvae were obtained from the natural spawning of adult fish (4 years old) raised exclusively on artificial feed from fingerlings [38]. Spawning was carried out in a square tank measuring 1600 L using artificial spawning substrates, namely, metal frames covered with nylon mesh. After spawning, the eggs were incubated on the frames in air-incubated spray chambers; the development of eggs occurred in a “water mist” environment [39]. During the final stages of embryonic development, the frames with the fish embryos were moved to water-circulated tanks, where the larvae hatched. Once the larvae could swim in the horizontal plane, they were transferred into 4 square meter tanks with a water depth of 0.25 m and began to feed on natural lake zooplankton (see the Zooplankton sampling and taxon determination subsection below).
The larvae were reared at an initial density of 25 specimens per liter (around 2000 larvae per tank) in accordance with previous recommendations [28]. The plankton density in the fish tank was maintained at a level of at least 1000 individuals per liter, which is sufficient to support a high growth rate for perch larvae [40]. To determine the average weight of individual larvae, a sample of 200–250 larvae was taken at the beginning of the experiment. Three samples were collected, and the average weight was calculated. The larvae were sacrificed with clove oil, dried on filter paper, and weighed on a scale with a resolution of 1 mg. The number of larvae in each sample was also counted. During the study, body weight was determined in a smaller number of specimens (30–35). The survival rate of the larvae raised on zooplankton ranged from 3.6% to 4.4%, averaging 3.8 ± 0.22%. Immediately after capture from the lake, they were fed zooplankton in equal portions four times a day, from 8:00 a.m. to 8:00 p.m., every 4 h. The photoperiod (up to 100 lux) and water temperature remained at natural levels throughout the experiment. The water temperature ranged from 16 to 21 °C. These experiments were carried out in three replications for statistical significance.

2.2. Zooplankton Sampling and Taxon Determination

The zooplankton used for feeding the larvae were collected from the coastal area of Sukhodolskoye Lake at a depth of up to 0.5 m using a net with a 60 cm diameter made from harvested sieve tissue with a mesh size of 93 μm. Zooplankton samples were obtained by filtering 100 L of water through an Apstein net with a mesh size of 93 μm. The samples were fixed in a 4% formaldehyde solution, and the organisms were identified to the high-rank taxon level (Copepoda, Rotifera, or Cladocera) [41].
The first zooplankton sampling was conducted at the beginning of the transition of pikeperch larvae to active external feeding, which was used as the starting point for the experiment. Subsequently, sampling was performed every 6 days. During the initial stages of the experiment (probe 1), the zooplankton were sieved using a harvesting sieve with a mesh size of 0.2 mm. On day 7 (probe 2), the mesh size was increased to 0.5 mm, and on day 13 (probe 3), it was further increased to 0.8 mm. Finally, on day 19 (probe 4), all zooplankton samples were collected without sieving. By sieving, it was possible to analyze the size groups of zooplankton that could potentially be available for fish larvae during sampling.

2.3. Biochemical Analysis of Zooplankton Species

Several chemical analysis methods were used to determine the relative content of liquid, dry matter, lipids (using the Folch method [42]), protein (using the Kjeldahl method [43]), minerals (by burning the sample in a muffle furnace at 550 °C), and nitrogen-free extracts (NFEs) via calculation [44]. Each probe was analyzed three times.
The fatty acid composition of zooplankton lipids was determined using gas–liquid chromatography. For this purpose, zooplankton probes were collected and transported to the laboratory in an insulated box, where the temperature was kept at the same level as in the natural environment. The probes were processed immediately after sampling. Each probe weighed at least 1 g and was homogenized. Lipids were extracted using the method described by Hara and Radin [45], which involved using hexane–isopropanol (3:2) and then washing the extract with a sodium sulfate solution to remove non-lipid impurities. Acetyl chloride in methanol at a concentration of 10% was used to methylate the fatty acids.
Chromatographic separation was carried out on a Crystal 5000.2 gas chromatograph (CHROMATEC, Yoshkar-Ola, Russia) equipped with a flame ionization detector (FID). A capillary column (CR-FAME, 100 m × 0.25 mm × 0.2 μm; CHROMATEC, Russia) was used. The analysis was performed at a temperature of 160 °C for 5 min, followed by an increase in temperature to 220 °C at a rate of 2 °C/min, and then holding at the final temperature for an additional 5 min. The peaks were determined by comparing the relative retention time of the FAME sample standard. Two reference mixtures, 20A and GLC-68A (NuChek Prep, Elysian, MN, USA), were used to check the change in the detector response to different FAMEs.
Before analyzing the amino acid composition in zooplankton proteins, the probes were hydrolyzed in 6N HCl at 110 °C for 24 h in a nitrogen atmosphere. The amino acid content was determined using a Shimadzu LC-10AS system (Shimadzu, Kyoto, Japan), which used a C-18 polystyrene column and an FL 6A fluorescence detector with CR6A ChromPac recorder software. Amino acid standards, A2161 (Sigma-Aldrich, St. Louis, MO, USA), were used to calibrate the analyzer and calculate the amino acid composition in the samples. To calculate tryptophan, the samples were digested with 5% NaOH for 24 h and then neutralized to pH 7.0 with 6N HCl.

2.4. Hydrochemical Parameters of the Water in the Experiment and Their Monitoring

Hydrochemical analysis of the water probes was carried out in accordance with the APHA [46]. The probes were collected using a Rutner bathometer, with a volume of 1 dm3, from a depth of 0.5 m in accordance with the zooplankton sampling (on days 1, 7, 13, and 19 during larval feeding).
Several water parameters were measured:
  • The content of phosphorus phosphates (PO4–P) was analyzed using the Murphy–Riley method [47].
  • Free CO2 was calculated using the titrimetric method with a 0.02 N Na2CO3 solution.
  • Alkalinity was determined using potentiometric titration with 0.02 N H2SO4.
  • Nitrite-N (NO2-N) and nitrate nitrogen (NO3-N) contents were measured using spectrophotometry with Bendschneider and Robinson solutions.
  • Total nitrogen was analyzed using spectrophotometry with Nessler’s reagent.
  • Oxygen dissolved in water was measured by OxyGuard Polaris C (OxyGuard International A/S, Farum, Denmark).
  • pH level was measured using an MP-125 digital pH meter (Mettler Toledo, Columbus, OH, USA).
The hydrochemical parameters showed slight changes, but they remained within the normal limits for fishery reservoirs during the experiment (see Table 1). This ensured that the pikeperch larvae were in optimal conditions.

2.5. Statistical Analysis of the Data

Statistical data processing was carried out using the Statistica 6.0 software package. Tables show the arithmetic mean (M) and the standard deviation (SD). Homogeneity of variances was tested using Levene’s test, and differences between treatments were analyzed using a one-way analysis of variance (ANOVA) and a Scheffe post hoc test. Differences were considered significant if the p-value was lower than 0.05.

3. Results

3.1. Taxonomic Diversity of Zooplankton from Sukhodolskoye Lake

The taxonomic diversity of the zooplankton sampled from Sukhodolskoye Lake and sieved during the experiment is shown in Figure 2. Rotifers (approximately 52%) dominated in probe 1, followed by copepods and cladocerans—approximately 27% and 21%, respectively. In probes 2 and 3, cladocerans accounted for more than 93% of the taxon diversity, with rotifers accounting for less than 1% and copepods 4–6%. In probe 4, the cladoceran proportion was approximately 61%, with the rotifer proportion at approximately 20% and the copepod proportion at approximately 19%. Figure 3 illustrates the change in larval size during the experiment at 3, 9, 15and 21 days post-hatching.

3.2. Biochemical Composition of Zooplankton from Sukhodolskoye Lake

The biochemical composition of the zooplankton throughout the entire experimental period was generally homogeneous, with the exception of a higher content of lipids and dry matter in the first two probes (probes 1 and 2), compared to the two following ones (probes 3 and 4)—on average, 24.8% versus 22.4% for lipids and 10.73% versus 9.23% for dry matter, respectively (Table 2).

3.3. Fatty Acid Composition of the Lipids in Zooplankton from Sukhodolskoye Lake

There were significant differences in the fatty acid (FA) composition of the zooplankton lipids during the experiment. In probe 1, half of which was represented by rotifers (Figure 2), unsaturated fatty acids (UFAs) were dominant—42.37% of the total fatty acids, of which n-3 accounted for 14.01% and n-6 accounted for 28.36%. Among the n-6 UFAs, arachidonic acid (ARA) was the most represented (21.14%). Saturated (SFAs) and monounsaturated (MUFAs) fatty acids accounted for 27.71% and 23.69% of the total, respectively (Table 3).
In probes 2 and 3, which were almost entirely composed of Cladocera species (Figure 2), the most representative class was SFAs, accounting for 33.28% and 38.65%, followed by MUFAs at 33.04% and 30.58%. UFAs accounted for 27.63% and 25.94%, respectively. In probe 4, which was composed of 60.95% cladocerans, 19.90% rotifers, and 19.15% copepods (Figure 2), half of the lipids were SFAs (50.66%), followed by MUFAs (25.69%) and UFAs (16.44%) (Table 3).
Palmitic acid (C16:0), which ranged from 19.25% to 32.68% in the SFA class, was a common feature of the fatty acid profile in the different zooplankton probes. Among monoenoic acids, 18:1 n-9 and 20:1 n-9 provided the main contributions at 4.91–6.19% and 4.46–12.33%, respectively.
The content of n-3 UFAs during the entire experiment was relatively low, ranging from 11.91% to 16.92%. Maternal alpha-linolenic acid (ALA), 18:3 n-3, was the most representative fatty acid in this group, with a concentration of 5.61–8.53%. DHA, the most physiologically significant n-3 UFA, was present in small amounts, ranging from 0.70% to 2.82%. Eicosapentaenoic acid (EPA) was also present at a low level, with a range of 1.64% to 4.44%.
The percentage of n-6 UFAs decreased during the experiment, dropping from 28.36% to 4.53%. Linoleic acid (LA), the most common n-6 fatty acid, ranged from 3.05% to 6.59%, while ARA, with a starting concentration of 21.14% in probe 1, decreased to a range of 1.48% to 4.31% in subsequent probes.

3.4. Amino Acid Composition of Zooplankton from Sukhodolskoye Lake

The amino acid composition of the zooplankton samples collected during the observation period showed significant differences between samples (Table 4). Probe 1, which consisted of 50% rotifers, had the lowest levels of arginine, threonine, histidine, and valine but a high content of lysine.
The composition of essential amino acids (EAAs) in probes 2 and 3, which were represented mostly by the Cladocera species of zooplankton, was similar and characterized by relatively high contents of arginine, lysine, and histidine. Probe 4, which contained Cladocera, Rotifera, and Copepoda species at a ratio of 3:1:1, had the highest levels of threonine, valine, isoleucine, and leucine among the studied probes. The low level of methionine, which did not exceed 1.1% in any of the probes, was common to all of them.
Among EAAs, alanine was the most abundant amino acid, accounting for 19–25% of the total amino acid content. Aspartic acid was the second most prevalent in the first two probes, while glutamic acid was the next most abundant in the last two. The proline content was lower in the first two probes, being approximately half of that in probes 3 and 4 (Table 4).
Due to the lack of information about the amino acid requirements of pikeperch larvae, we compared the amino acid composition of zooplankton with the diets of early juvenile pikeperches based on data from a closely related European perch. The amino acid composition in the body of P. fluviatilis was found to be very similar to that of S. lucioperca, suggesting that these two species have similar nutritional requirements [48,49].
Table 4. Amino acid composition of the zooplankton sampled from Sukhodolskoye Lake (in percentages) and dietary requirements for the larvae of European perch (Perca fluviatilis). Three replicates for each probe were used.
Table 4. Amino acid composition of the zooplankton sampled from Sukhodolskoye Lake (in percentages) and dietary requirements for the larvae of European perch (Perca fluviatilis). Three replicates for each probe were used.
ParameterProbe 1Probe 2Probe 3Probe 4Dietary Requirements for the Larvae of European Perch [50]
Fish larval developmental stage, days post-hatching (dph)391521-
Water temperature, °C15.918.521.521.7-
Essential amino acids (EAAs), %
Arginine1.9 ± 0.06 a5.1 ± 0.06 b5.4 ± 0.05 c3.7 ± 0.03 d4.0
Lysine6.9 ± 0.07 a6.5 ± 0.06 b6.2 ± 0.06 c3.5 ± 0.03 d5.2
Phenylalanine3.0 ± 0.05 a2.9 ± 0.04 a3.5 ± 0.05 b3.3 ± 0.06 c2.8
Methionine1.1 ± 0.06 a,d0.7 ± 0.04 b0.9 ± 0.09 c,d1.0 ± 0.04 d1.9
Threonine4.5 ± 0.09 a5.1 ± 0.11 b5.0 ± 0.06 b5.9 ± 0.08 c3.3
Histidine5.4 ± 0.07 a6.2 ± 0.06 b7.6 ± 0.05 c6.4 ± 0.04 b2.0
Valin5.7 ± 0.11 a6.3 ± 0.06 b7.3 ± 0.07 c8.9 ± 0.09 d3.8
Isoleucine4.1 ± 0.06 a4.0 ± 0.04 a5.1 ± 0.05 b6.2 ± 0.07 c3.3
Leucine4.8 ± 0.04 a4.9 ± 0.06 a5.6 ± 0.07 b5.7 ± 0.06 b5.0
ΣEAA37.4 ± 0.7241.7 ± 0.9645.6 ± 0.8844.6 ± 1.0131.3
Nonessential amino acids (NEAAs), %
Alanine25.1 ± 0.14 a22.4 ± 0.17 b19.3 ± 0.22 c18.9 ± 0.18 cn/d
Aspartic acid13.2 ± 0.09 a12.8 ± 0.10 b9.0 ± 0.09 c8.7 ± 0.07 dn/d
Glutamic acid8.9 ± 0.05 a8.7 ± 0.06 b9.8 ± 0.08 c9.8 ± 0.07 cn/d
Glycine4.6 ± 0.03 a4.2 ± 0.05 b3.4 ± 0.04 c3.9 ± 0.03 dn/d
Oxyproline0.5 ± 0.01 a0.5 ± 0.02 a0.8 ± 0.02 b0.9 ± 0.02 cn/d
Proline2.9 ± 0.02 a2.5 ± 0.03 b5.4 ± 0.05 c5.7 ± 0.05 dn/d
Serin6.0 ± 0.04 a5.3 ± 0.07 b6.1 ± 0.04 c6.1 ± 0.06 cn/d
Tyrosine1.4 ± 0.02 a1.9 ± 0.02 b0.6 ± 0.01 c1.4 ± 0.02 an/d
ΣNEAA62.6 ± 0.6459.2 ± 0.8152.5 ± 0.7555.4 ± 0.70n/d
a,b,c,d Values (mean ± SD) in the same row with different letters indicate significant differences (p ≤ 0.05). n/d, not defined.

4. Discussion

Data on the biochemical composition of lake zooplankton from the natural range of pikeperch provide information on the nutritional requirements of larvae during early post-embryonic development since, in aquaculture, pikeperch larvae die when only dry food is used as a starter feed. The high protein content in lake zooplankton (68–70%), which did not significantly change over the course of the experiment, is consistent with previously published data obtained mainly on Cladocera species of zooplankton [30,51,52]. This indicates that the protein content in the zooplankton met the dietary requirements of early pikeperch larvae, estimated at 55% based on the literature [22].
During the experimental period, there was a significant decrease in the dry matter content of the zooplankton. The average dry matter content in the first two probes was 10.7%, but in the subsequent probes 3 and 4, it decreased to 9.2%. This decrease in dry matter correlates with a corresponding decrease in lipids from 24.8% at the beginning of the experiment to 22.4%. This decrease in lipids seems to be due to an increase in water temperature, from an average of 17.5 °C to 20.7 °C, and can be interpreted as a response by small organisms to adapt to cold-water environments [53].
In turn, the warming of the water during the experimental period may have contributed to a decrease in the UFA content, from 42.37% to 16.44% of the total fatty acid content. This trend in our results is consistent with the findings of Nanton and Castell [54], who observed significantly higher levels of UFAs in zooplankton lipids at 6 °C compared to 20 °C. This supports the hypothesis of homeoviscous adaptation, which suggests that the maintenance of cell membrane fluidity at low temperatures is achieved through the accumulation of UFAs [55]. Despite the overall decrease in UFAs during the observations, the n-3/n-6 ratio increased from 0.5 to 2.6 during the experiment.
It is important to note that the optimal ratio of fatty acid components in lipids plays a crucial role in the normal physiological state of fish larvae. This is determined by both dietary factors and the ability of the organism to modify it according to its living conditions [56,57,58]. For example, for pikeperch larvae, the ALA/LA ratio should be 1:1.4, and the DHA/EPA ratio should be 5:1 [59], with the sum of DHA and EPA satisfying the nutritional requirements of early pikeperch larvae being at least 3.5% of the total fatty acid content [14]. The optimal n-3/n-6 ratio ranges from 0.8:1 to 2.5:1 based on the requirements of the European perch, which is closely related to the pikeperch [60].
Based on the data presented, it can be concluded that the fatty acid composition of the studied lake zooplankton generally corresponds to the nutritional requirements of pikeperch larvae in the early stages of development. An exception is the low content of DHA, which was found to range from 0.70% to 2.82% of the total fatty acids. This is typical for freshwater zooplankton, particularly those that feed on phytoplankton [61]. Phytoplankton feeding is indicated by high levels of ALA and LA, the main unsaturated fatty acids in freshwater algae [62]. In this study, ALA and LA were found to be more abundant in the zooplankton lipids than EPA and DHA, with levels up to 8.53% and 6.59%, respectively (see Table 3), while EPA and DHA ranged up to 4.44% and 2.82%.
There was a high content of ARA in the smallest forms of zooplankton, half of which were represented by rotifers (Table 3, probe 1), and this characterizes zooplankton as a phytoplanktivorous group. This content of ARA has previously been noted in some freshwater green microalgae, such as Lobosphaera incisa, where it reached 50% [63]. The important role of ARA in fish reproduction and its beneficial effect on the quality of offspring (eggs and larvae in the early stages of development [64]) are well known and also documented in studies on juveniles of marine Percidae species: ARA increases stress tolerance in these species [65]. It is likely that the presence of ARA in zooplankton contributes to the adaptation of pikeperch larvae to changing environmental conditions and increases their survival rate.
DHA, EPA, and ARA are the most significant long-chain UFAs necessary for physiological processes. These UFAs are found in relatively significant amounts in newly hatched pikeperch larvae and continue to be present in the body during prolonged periods of starvation [21,66]. Based on this information, it has been suggested that the contents of individual non-essential fatty acids in pikeperch larvae can serve as a guideline for dietary requirements. However, we suggest that the presence of certain fatty acids in large quantities in pikeperch larvae during early development may indicate their importance in physiological processes rather than reflecting the actual requirements of the organism. The high content of UFAs in larvae is likely due to their adaptive properties, formed by the maternal organism through eggs and the yolk sac to overcome the deficiency of these physiologically significant fatty acids in the early stages of development, especially during the period of feeding on zooplankton, which are poor in long-chain UFAs.
The amino acid composition of the zooplankton during the experimental period varied significantly, which may be attributed to the diverse community of zooplankton species in different probes (Figure 2). Overall, the amino acid profiles of the zooplankton selected for analysis at various stages of pikeperch larval development met the specific nutritional requirements. According to Fiogbe and coauthors [48], pikeperches have increased dietary requirements for leucine, threonine, and valine, all of which were present in the zooplankton studied in sufficient quantities (Table 4). Lysine, a limiting amino acid in fish diets [67], was also found in sufficient amounts in the lake zooplankton to meet juvenile perch nutritional requirements—more than 6% of the total amino acids required by the larvae. Only probe 4 had a lower lysine content of 3.5% in this experiment.
Arginine, a functional amino acid involved in the immune and antioxidant systems [68,69], was present at high levels in the zooplankton during the experiment, except in the initial probe, where its content was 1.9%. On average, arginine accounted for 4.0% of the total amino acid content in the zooplankton over the experimental period, which corresponds to the requirements of perch fish (Table 4). Other essential amino acids, such as phenylalanine, histidine, and isoleucine, were also present in excess in the zooplankton, averaging 3.2%, 5.4%, and 4.0%, respectively, compared to their requirements of 2.8%, 2.0%, and 3.3% in perch fish.
The only essential amino acid found to be deficient in the zooplankton during the experiment was methionine. This amino acid made up between 0.7% and 1.1% of the total amino acid content, but its overall requirement is 1.9%. Generally, low levels of methionine are characteristic of freshwater zooplankton from different geographical regions [30,52,68,69,70,71]. This could limit their use as a sole food source for perch larval rearing in the early stages of development, as it could lead to a deficiency in the larvae’s diet. It is also important to note that cysteine, which was not measured in this study and is synthesized from methionine through the transsulfuration pathway, can compensate for the methionine requirement of vertebrates [72]. Additionally, in the bodies of Eurasian perch larvae weighing one milligram, methionine accounts for a relatively large proportion of total amino acids (2.5%) [48], which could compensate for any lack of this amino acid in their starter feed.
The main focus of fish protein nutrition is on essential amino acids, while the composition of non-essential amino acids is not strictly regulated in the diet. This is because non-essential amino acids can be transformed into other amino acids through a process called transamination, which involves the use of glutamic acid as an amino group donor [73]. Glutamic acid is essential for this process, and its content in zooplankton varies from 9% to 10%. However, the requirements of pikeperch larvae for glutamic acid and other non-essential amino acids have not been well studied.

5. Conclusions

The size fractions of freshwater zooplankton were studied using oligotrophic Sukhodolskoye Lake in the northern part of Eastern Europe as an example. These zooplankton, available for feeding pikeperch larvae at various stages of development, showed significant species diversity.
The high protein content of the zooplankton (68–70%) remained consistent throughout the study, which was in line with previous research and met the estimated dietary requirement of 55% protein for pikeperch larvae. There was a noticeable decrease in both the dry matter and lipid content of the zooplankton, likely due to increased water temperatures, which affects the fatty acid composition, particularly the levels of unsaturated fatty acids. Although the overall levels of UFAs decreased, the n-3/n-6 ratio improved, potentially enhancing the nutritional value for larval pikeperch. However, low levels of DHA could be a limiting factor, as it is crucial for larval development.
The amino acid profile of the zooplankton generally met the dietary needs of pikeperch larvae, providing sufficient levels of essential amino acids such as leucine, threonine, and valine. The methionine levels, however, were found to be deficient, potentially limiting optimal growth and development. The presence of arachidonic acid (ARA) in zooplankton may help pikeperch larvae cope with environmental changes. This acid is thought to enhance their resilience, while the overall amino acid composition of zooplankton is vital for their physiological needs.
Thus, the biochemical parameters of zooplankton generally meet the dietary requirements of early pikeperch larvae, and the lack of methionine and DHA can be compensated for by their high content in the bodies of early pikeperch larvae. The data presented in this study can be used to understand the nutritional requirements of pikeperch larvae and to develop new artificial starter feeds for freshwater aquaculture.

Author Contributions

Conceptualization, A.L., A.K. and A.T.; methodology, A.L., A.K. and A.T.; formal analysis, A.L. and A.N.; investigation, A.L., A.K. and A.T.; resources, A.L. and A.Z.; writing—original draft preparation, A.L. and A.N.; writing—review and editing, A.L., A.Z. and A.N.; visualization, A.N.; supervision, A.L.; project administration, A.L.; funding acquisition, A.L. and A.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Russian Science Foundation, grant number 24-76-10054.

Institutional Review Board Statement

The experiment on fish in the current research was performed in accordance with legislation of the Russian Federation. The method corresponds to contemporary recommended practices (EU Directive 2010/63/EU) and was approved by the Animal Ethics Committee of the State Research Institute of Lake and River Fisheries (St. Petersburg, Russia). All of the procedures were carried out in accordance with the guidelines of the Regulations for the Administration of Laboratory Animals (Decree No. 2 of the State Science and Technology Commission of the People’s Republic of China, 14 November 1988), and were approved by the Animal Ethics Committee of Zhejiang Ocean University (Zhoushan, China).

Informed Consent Statement

Not applicable.

Data Availability Statement

All of the data are represented in the manuscript.

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

The following abbreviations are used in this manuscript:
ALAAlpha-linolenic acid
APHAAmerican Public Health Association
ARAArachidonic acid
DHADocosahexaenoic acid
DPHDays post-hatching
EAAEssential amino acid
EPAEicosapentaenoic acid
FAFatty acid
FIDFlame ionization detector
LALinolenic acid
MPCMaximum permissible concentration
MUFAMonounsaturated fatty acid
NFENitrogen-free extract
NO2-NNitrite-N
NO3-NNitrate nitrogen
NEAANonessential essential amino acid
PO4–PPhosphorus phosphate
SFASaturated fatty acid
UFAUnsaturated fatty acid

References

  1. Alexi, N.; Byrne, D.V.; Nanou, E.; Grigorakis, K. Investigation of sensory profiles and hedonic drivers of emerging aquaculture fish species. J. Sci. Food Agric. 2018, 98, 1179–1187. [Google Scholar] [CrossRef] [PubMed]
  2. Colchen, T.; Gisbert, E.; Krauss, D.; Ledoré, Y.; Pasquet, A.; Fontaine, P. Improving pikeperch larviculture by combining environmental, feeding and populational factors. Aquac. Rep. 2020, 17, 100337. [Google Scholar] [CrossRef]
  3. Dalsgaard, J.; Lund, I.; Thorarinsdottir, R.; Drengstig, A.; Arvonen, K.; Pedersen, P.B. Farming different species in RAS in Nordic countries: Current status and future perspectives. Aquac. Eng. 2013, 53, 2–13. [Google Scholar] [CrossRef]
  4. Colchen, T.; Ledoré, Y.; Fontaine, P.; Teletchea, F.; Pasquet, A. Larval pikeperch Sander lucioperca cannibals are more efficient predators on zebrafish Danio rerio than non-cannibals. Aquaculture 2023, 575, 739756. [Google Scholar] [CrossRef]
  5. Kestemont, P.; Dabrowski, K.; Summerfelt, R.C. Biology and Culture of Percid Fishes: Principles and Practices; Kestemont, P., Dabrowski, K., Summerfelt, R.C., Eds.; Springer: Berlin/Heidelberg, Germany, 2015. [Google Scholar]
  6. Klein Breteler, J. Intensive culture of pike-perch fry with live food. Intensive culture of pikeperch fry with live food. In Aquaculture—A Biotechnology in Progress; De Pauw, N., et al., Eds.; European Aquaculture Society: Bredene, Belgium, 1989; Volume 1, pp. 203–207. [Google Scholar]
  7. Steffens, W.; Geldhauser, F.; Gerstner, P.; Hilge, V. German experiences in the propagation and rearing of fingerling pikeperch (Stizostedion lucioperca). Ann. Zool. Fenn. 1996, 33, 627–634. [Google Scholar]
  8. Mani-Ponset, L.; Diaz, J.-P.; Schlumberger, O.; Connes, R. Development of yolk complex, liver and anterior intestine in pike-perch larvae, Stizostedion lucioperca (Percidae), according to the first diet during rearing. Aquat. Living Resour. 1994, 7, 191–202. [Google Scholar] [CrossRef]
  9. Nyina-Wamwiza, L.; Xu, X.L.; Blanchard, G.; Kestemont, P. Effect of dietary protein, lipid and carbohydrate ratio on growth, feed efficiency and body composition of pikeperch Sander lucioperca fingerlings. Aquac. Res. 2005, 36, 486–492. [Google Scholar] [CrossRef]
  10. Ostaszewska, T. Developmental changes of digestive system structures in pike-perch (Sander lucioperca L.). Electron. J. Ichthyol. 2005, 2, 65–78. [Google Scholar]
  11. Dabrowski, K. The role of proteolytic enzymes in fish digestion. Cultiv. Fish Fry Live Food 1979, 4, 107–126. [Google Scholar]
  12. Lauff, M.; Hofer, R. Proteolytic enzymes in fish development and the importance of dietary enzymes. Aquaculture 1984, 37, 335–346. [Google Scholar] [CrossRef]
  13. Srichanun, M.; Tantikitti, C.; Vatanakul, V. Digestive enzyme activity during ontogenetic development and effect of live feed in green catfish larvae (Mystus nemurus Cuv. & Val.). Songklanakarin J. Sci. Technol. 2012, 34, 247–254. [Google Scholar]
  14. El Kertaoui, N.; Lund, I.; Assogba, H.; Domínguez, D.; Izquierdo, M.S.; Baekelandt, S.; Cornet, V.; Mandiki, S.N.M.; Montero, D.; Kestemont, P. Key nutritional factors and interactions during larval development of pikeperch (Sander lucioperca). Sci. Rep. 2019, 9, 7074. [Google Scholar] [CrossRef] [PubMed]
  15. Kestemont, P.; Henrotte, E. Nutritional Requirements and Feeding of Broodstock and Early Life Stages of Eurasian Perch and Pikeperch. In Biology and Culture of Percid Fishes: Principles and Practices; Kestemont, P., Dabrowski, K., Summerfelt, R.C., Eds.; Springer: Dordrecht, The Netherlands, 2015; pp. 539–564. [Google Scholar]
  16. Barrows, F.T.; Lellis, W.A.; Nickum, J.G. Intensive Culture of Larval Walleyes with Dry or Formulated Feed: Note on Swim Bladder Inflation. Progress. Fish-Cult. 1988, 50, 160–166. [Google Scholar] [CrossRef]
  17. Antalfi, A. Propagation and rearing of perch in pond culture. EIFAC Tech. Pap. 1979, 35, 120–125. [Google Scholar]
  18. Beyerle, G.B. Summary of Attempts to Raise Walleye Fry and Fingerlings on Artificial Diets, with Suggestions on Needed Research and Procedures to be Used in Future Tests. Progress. Fish-Cult. 1975, 37, 103–105. [Google Scholar] [CrossRef]
  19. Ruuhijärvi, J.; Virtanen, E.; Salminen, M.; Muyunda, M. The growth and survival of pike-perch, Stizostedion lucioperca L., larvae fed on formulated feeds. In Proceedings of the International Symposium on Fish and Crustacean Larviculture, Gent, Belgium, 27–30 August 1991; pp. 154–156. [Google Scholar]
  20. Schlumberger, O.; Proteau, J. Production de juveniles de sandre (Stizostedion lucioperca). Aqua Rev. 1991, 36, 25–28. [Google Scholar]
  21. Bischoff, A.A.; Kubitz, M.; Wranik, C.M.; Pfefferkorn, H.; Augustin, C.B.; Hagen, W.; Palm, H.W. Fatty acid utilization of pikeperch (Sander lucioperca (Linnaeus, 1758)) larvae under starvation conditions during early development. Bull. Fish Biol. 2017, 17, 59–73. [Google Scholar]
  22. Kestemont, P.; Xueliang, X.; Hamza, N.; Maboudou, J.; Imorou Toko, I. Effect of weaning age and diet on pikeperch larviculture. Aquaculture 2007, 264, 197–204. [Google Scholar] [CrossRef]
  23. Kowalska, A.; Zakęś, Z.; Demska-Zakęś, K. The impact of feeding on the results of rearing larval pikeperch, Sander lucioperca (L.), with regard to the development of the digestive tract. Electron. J. Pol. Agric. Univ. Fish. 2006, 9. Available online: http://www.ejpau.media.pl/volume9/issue2/abs-5.html (accessed on 23 January 2025).
  24. Ljubobratović, U.; Fazekas, G.; Koljukaj, A.; Ristović, T.; Vass, V.; Ardó, L.; Stanisavljević, N.; Vukotić, G.; Pešić, M.; Milinčić, D.; et al. Pike-perch larvae growth in response to administration of lactobacilli-enriched inert feed during first feeding. Aquaculture 2021, 542, 736901. [Google Scholar] [CrossRef]
  25. Ljubobratović, U.; Kucska, B.; Feledi, T.; Poleksić, V.; Marković, Z.; Lenhardt, M.; Peteri, A.; Kumar, S.; Rónyai, A. Effect of weaning strategies on growth and survival of pikeperch, Sander lucioperca, larvae. Turk. J. Fish. Aquat. Sci. 2015, 15, 325–331. [Google Scholar] [CrossRef] [PubMed]
  26. Rønfeldt, J.; Nielsen, J. Filling of Gas Bladder, Growth and the Survival in Pikeperch Larvae (Sander lucioperca) in Intensive Aquaculture. Master’s Thesis, University of Copenhagen, Copenhagen, Denmark, 2010. [Google Scholar]
  27. Steenfeldt, S.; Vestergaard, M.; Overton, J.; Paulsen, H.; Larsen, V.; Henriksen, N. Development of intensive rearing of pikeperch in Denmark. Den. Anon. Hirtshals. 2010, 303–323. Available online: https://orbit.dtu.dk/files/6581395/228-2010_Videreudvikling-af-intensivt-opdraet-af-sandart-i-Danmark.pdf (accessed on 23 January 2025). (In Danish).
  28. Szkudlarek, M.; Zakęś, Z. Effect of stocking density on survival and growth performance of pikeperch, Sander lucioperca (L.), larvae under controlled conditions. Aquac. Int. 2007, 15, 67–81. [Google Scholar] [CrossRef]
  29. Czesny, S.; Kolkovski, S.; Yackey, C.; Dabrowski, K. The effects of (n-3) HUFA enriched Artemia nauplii on growth, survival, and quality of walleye Stizostedion vitreum fry. Aquaculture 1998, 178, 103–115. [Google Scholar] [CrossRef]
  30. Watanabe, T.; Kitajima, C.; Fujita, S. Nutritional values of live organisms used in Japan for mass propagation of fish: A review. Aquaculture 1983, 34, 115–143. [Google Scholar] [CrossRef]
  31. Hamza, N.; Kestemont, P.; Khemis, I.B.; Mhetli, M.; Cahu, C. Effect of different sources and levels of dietary phospholipids on performances and fatty acid composition of pikeperch (Sander lucioperca) larvae. Aquac. Nutr. 2012, 18, 249–257. [Google Scholar] [CrossRef]
  32. Lund, I.; Skov, P.V.; Hansen, B.W. Dietary supplementation of essential fatty acids in larval pikeperch (Sander lucioperca); short and long term effects on stress tolerance and metabolic physiology. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 2012, 162, 340–348. [Google Scholar] [CrossRef]
  33. Ostaszewska, T.; Boruta, A. The effect of diet on the fatty acid composition and liver histology of pikeperch (Sander lucioperca (L.)) larvae. Fish. Aquat. Life 2006, 14, 53–66. [Google Scholar]
  34. Izquierdo, M.; Koven, W. Lipids. In Larval Fish Nutrition; John Wiley & Sons.: Hoboken, NJ, USA, 2011; pp. 47–81. [Google Scholar]
  35. Schlumpberger, W. Untersuchungen zur Entwicklung eines industrie-mäβigen Verfahrens für die Produktion von vorgestreckten Zandern (Stizustedion lucioperca [L.]). Ph.D. Thesis, Humboldt-Univ., Berlin, Germany, 1979; p. 232. [Google Scholar]
  36. Peterka, J.; Matína, J.; Lipka, J. The diet and growth of larval and juvenile pikeperch (Stizostedion lucioperca (L.)): A comparative study of fishponds and a reservoir. Aquac. Int. 2003, 11, 337–348. [Google Scholar] [CrossRef]
  37. Specziár, A. First Year Ontogenetic Diet Patterns in Two Coexisting Sander Species, S. lucioperca and S. volgensis in Lake Balaton. Hydrobiologia 2005, 549, 115–130. [Google Scholar] [CrossRef]
  38. Lyutikov, A.A.; Korolev, A.E.; Shumilina, A.K.; Lukina, Y.N.; Vylka, M.M.; Prishchepa, A.S. Comparative Characteristics of the Physiological State of Pikeperch (Sander Lucioperca) from Various Habitat Conditions: Lake (Natural Habitat), Ponds, and Fish Farm Cages. Contemp. Probl. Ecol. 2024, 17, 208–218. [Google Scholar] [CrossRef]
  39. Woynarovich, E. Aufzucht der Zanderlarven bis zum Raubfischalter. Z. Fur Fisch. 1960, 9, 73–83. [Google Scholar]
  40. Wang, N.; Eckmann, R. Effects of temperature and food density on egg development, larval survival and growth of perch (Perca fluviatilis L.). Aquaculture 1994, 122, 323–333. [Google Scholar] [CrossRef]
  41. Alekseev, V.R.; Tsalolikhin, S.A. (Eds.) Taxonomic Key of Zooplankton and Freshwater Zoobenthos of European Russia; KMK Scientific Press: Moscow, Russia, 2010; Volume 1, p. 495. [Google Scholar]
  42. Eggers, L.F.; Schwudke, D. Liquid Extraction: Folch. In Encyclopedia of Lipidomics; Wenk, M.R., Ed.; Springer: Dordrecht, The Netherlands, 2016; pp. 1–6. [Google Scholar]
  43. Sáez-Plaza, P.; José, N.M.; Sławomir, W.; Tadeusz, M.; Asuero, A.G. An Overview of the Kjeldahl Method of Nitrogen Determination. Part II. Sample Preparation, Working Scale, Instrumental Finish, and Quality Control. Crit. Rev. Anal. Chem. 2013, 43, 224–272. [Google Scholar] [CrossRef]
  44. AOAC. Official Methods of Analysis of the Association of Official Analytical Chemists, 16th ed.; AOAC International: Gaithersburg, MD, USA, 1998; Volume 1. [Google Scholar]
  45. Hara, A.; Radin, N.S. Lipid extraction of tissues with a low-toxicity solvent. Anal. Biochem. 1978, 90, 420–426. [Google Scholar] [CrossRef]
  46. APHA. Standard Methods for the Examination of Water and Wastewater, 17th ed.; American Public Health Association: Washington, DC, USA, 1989. [Google Scholar]
  47. Cho, Y.-H.; Nielsen, S.S. Phosphorus Determination by Murphy-Riley Method. In Food Analysis Laboratory Manual; Nielsen, S.S., Ed.; Springer International Publishing: Cham, Switzerland, 2017; pp. 153–156. [Google Scholar]
  48. Fiogbé, E.D.; Kestemont, P.; Mélard, C.; Micha, J.C. The effects of dietary crude protein on growth of the Eurasian perch Perca fluviatilis. Aquaculture 1996, 144, 239–249. [Google Scholar] [CrossRef]
  49. Zakes, Z.; Demska-Zakes, K. Intensive rearing of juvenile Stizostedion lucioperca (Percidae) fed natural and artificial diets. Ital. J. Zool. 1998, 65, 507–509. [Google Scholar] [CrossRef]
  50. Geay, F.; Kestemont, P. Feeding and Nutrition of Percid Fishes During Ongrowing Stages. In Biology and Culture of Percid Fishes: Principles and Practices; Kestemont, P., Dabrowski, K., Summerfelt, R.C., Eds.; Springer: Dordrecht, The Netherlands, 2015; pp. 587–622. [Google Scholar]
  51. Tay, S.H.; Rajbanshi, V.K.; Ho, W.H.; Chew, J.; Yap, E.A. Culture of cladoceran Moina micrura kurz using agroindustrial wastes. In Fish Nutrition Research in Asia, Proceedings of the Fourth Asian Fish Nutrition Workshop, Manila, Philippines, 3–8 September 1990; Asian Fisheries Society: Manila, Philippines, 1991; p. 1205. [Google Scholar]
  52. Yurkowski, M.; Tabachek, J.L. Proximate and amino acid composition of some natural fish foods. In Proceedings of the World Symposium on Finfish Nutrition and Fish Feed Technology, Hamburg, Germany, 20–23 June 1978; Heenemann Verlagsgesellschaft: Hamburg, Germany, 1979; pp. 435–448. [Google Scholar]
  53. Arts, M.T.; Robarts, R.D.; Evans, M.S. Energy Reserve Lipids of Zooplanktonic Crustaceans from an Oligotrophic Saline Lake In Relation to Food Resources and Temperature. Can. J. Fish. Aquat. Sci. 1993, 50, 2404–2420. [Google Scholar] [CrossRef]
  54. Nanton, D.A.; Castell, J.D. The effects of temperature and dietary fatty acids on the fatty acid composition of harpacticoid copepods, for use as a live food for marine fish larvae. Aquaculture 1999, 175, 167–181. [Google Scholar] [CrossRef]
  55. Farkas, T.; Herodek, S. The effect of environmental temperature on the fatty acid composition of crustacean plankton. J. Lipid Res. 1964, 5, 369–373. [Google Scholar] [CrossRef]
  56. Datsomor, A.K.; Zic, N.; Li, K.; Olsen, R.E.; Jin, Y.; Vik, J.O.; Edvardsen, R.B.; Grammes, F.; Wargelius, A.; Winge, P. CRISPR/Cas9-mediated ablation of elovl2 in Atlantic salmon (Salmo salar L.) inhibits elongation of polyunsaturated fatty acids and induces Srebp-1 and target genes. Sci. Rep. 2019, 9, 7533. [Google Scholar] [CrossRef] [PubMed]
  57. Navas, J.; Doste, S.; Carrillo, M.; Thrush, M.; Jara, J.; Bromage, N. Total lipid in the broodstock diet did not affect fatty acid composition and quality of eggs of sea bass (Dicentrarchus labrax L.). Sci. Mar. (Barc.) 2001, 65. [Google Scholar] [CrossRef]
  58. Tocher, D.R. Metabolism and Functions of Lipids and Fatty Acids in Teleost Fish. Rev. Fish. Sci. 2003, 11, 107–184. [Google Scholar] [CrossRef]
  59. Palm, H.W. Entwicklung Eines Zooplankton-Reaktors Zur Unterstützung Der Fischlarvenaufzucht Relevanter Zielfischarten in Mecklenburg Vorpommern (MV); Universität Rostock: Rostock, Germany, 2015; p. 67. [Google Scholar]
  60. Henrotte, É.; Overton, J.L.; Kestemont, P. Effects of dietary n-3 and n-6 fatty acids levels on egg and larval quality of Eurasian perch. Cybium 2008, 32, 271–272. [Google Scholar]
  61. Claus, C.; Benijts, F.; Vandeputte, G.; Gardner, W. The biochemical composition of the larvae of two strains of Artemia salina (L.) reared on two different algal foods. J. Exp. Mar. Biol. Ecol. 1979, 36, 171–183. [Google Scholar] [CrossRef]
  62. Bell, J.G.; Ghioni, C.; Sargent, J.R. Fatty acid compositions of 10 freshwater invertebrates which are natural food organisms of Atlantic salmon parr (Salmo salar): A comparison with commercial diets. Aquaculture 1994, 128, 301–313. [Google Scholar] [CrossRef]
  63. Bigogno, C.; Khozin-Goldberg, I.; Adlerstein, D.; Cohen, Z. Biosynthesis of arachidonic acid in the oleaginous microalga Parietochloris incisa (Chlorophyceae): Radiolabeling studies. Lipids 2002, 37, 209–216. [Google Scholar] [CrossRef]
  64. Bell, J.G.; Sargent, J.R. Arachidonic acid in aquaculture feeds: Current status and future opportunities. Aquaculture 2003, 218, 491–499. [Google Scholar] [CrossRef]
  65. Ganga, R.; Tort, L.; Acerete, L.; Montero, D.; Izquierdo, M.S. Modulation of ACTH-induced cortisol release by polyunsaturated fatty acids in interrenal cells from gilthead seabream, Sparus aurata. J. Endocrinol. 2006, 190, 39–45. [Google Scholar] [CrossRef]
  66. Abi-Ayad, S.M.E.A.; Boutiba, Z.; Mélard, C.; Kestemont, P. Dynamics of Total Body Fatty Acids During Early Ontogeny of Pikeperch (Sander lucioperca) Larvae. Fish Physiol. Biochem. 2004, 30, 129–136. [Google Scholar] [CrossRef]
  67. Small, B.C.; Soares JR, J.H. Quantitative dietary lysine requirement of juvenile striped bass Morone saxatilis. Aquac. Nutr. 2000, 6, 207–212. [Google Scholar] [CrossRef]
  68. Alam, M.S.; Teshima, S.-i.; Koshio, S.; Ishikawa, M. Arginine requirement of juvenile Japanese flounder Paralichthys olivaceus estimated by growth and biochemical parameters. Aquaculture 2002, 205, 127–140. [Google Scholar] [CrossRef]
  69. Costas, B.; Conceição, L.E.; Dias, J.; Novoa, B.; Figueras, A.; Afonso, A. Dietary arginine and repeated handling increase disease resistance and modulate innate immune mechanisms of Senegalese sole (Solea senegalensis Kaup, 1858). Fish Shellfish Immunol. 2011, 31, 838–847. [Google Scholar] [CrossRef] [PubMed]
  70. Mitra, G.; Mukhopadhyay, P.K.; Ayyappan, S. Biochemical composition of zooplankton community grown in freshwater earthen ponds: Nutritional implication in nursery rearing of fish larvae and early juveniles. Aquaculture 2007, 272, 346–360. [Google Scholar] [CrossRef]
  71. Srivastava, A.; Hamre, K.; Stoss, J.; Chakrabarti, R.; Tonheim, S.K. Protein content and amino acid composition of the live feed rotifer (Brachionus plicatilis): With emphasis on the water soluble fraction. Aquaculture 2006, 254, 534–543. [Google Scholar] [CrossRef]
  72. Di Buono, M.; Wykes, L.J.; Ball, R.O.; Pencharz, P.B. Dietary cysteine reduces the methionine requirement in men1234. Am. J. Clin. Nutr. 2001, 74, 761–766. [Google Scholar] [CrossRef]
  73. Lehninger, A.L. Biochemistry: The Molecular Basis of Cell Structure and Function; Worth Publishers New York: New York, NY, USA, 1975; Volume 2. [Google Scholar]
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Figure 1. Sukhodolskoye Lake. (A) Map showing Sukhodolskoye Lake, where studies on the taxonomic diversity and biochemical composition of zooplankton were conducted in 2022. The location of the fish farm “Forvat” is marked with a red triangle. (B) General view of the “Forvat” fish farm (LLC “Forvat”).
Figure 1. Sukhodolskoye Lake. (A) Map showing Sukhodolskoye Lake, where studies on the taxonomic diversity and biochemical composition of zooplankton were conducted in 2022. The location of the fish farm “Forvat” is marked with a red triangle. (B) General view of the “Forvat” fish farm (LLC “Forvat”).
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Figure 2. Taxonomic diversity of the zooplankton sampled from Sukhodolskoye Lake and sieved during the experiment. Zooplankton were collected using a series of sieves with different mesh sizes: 0.2 mm (probe 1—3 dph for pikeperch larvae), 0.5 mm (probe 2—9 dph for pikeperch larvae), 0.8 mm (probe 3—15 dph for pikeperch larvae), and without sieving (probe 4—21 dph for pikeperch larvae). Three replicates for each probe were used.
Figure 2. Taxonomic diversity of the zooplankton sampled from Sukhodolskoye Lake and sieved during the experiment. Zooplankton were collected using a series of sieves with different mesh sizes: 0.2 mm (probe 1—3 dph for pikeperch larvae), 0.5 mm (probe 2—9 dph for pikeperch larvae), 0.8 mm (probe 3—15 dph for pikeperch larvae), and without sieving (probe 4—21 dph for pikeperch larvae). Three replicates for each probe were used.
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Figure 3. Pikeperch larval growth (in mg) during the experiment. Probe 1—3 dph for pikeperch larvae (at 3 dph, larvae have approximately the same size and mass); probe 2—9 dph for pikeperch larvae; probe 3—15 dph for pikeperch larvae; probe 4—21 dph for pikeperch larvae. Three replicates for each probe were used.
Figure 3. Pikeperch larval growth (in mg) during the experiment. Probe 1—3 dph for pikeperch larvae (at 3 dph, larvae have approximately the same size and mass); probe 2—9 dph for pikeperch larvae; probe 3—15 dph for pikeperch larvae; probe 4—21 dph for pikeperch larvae. Three replicates for each probe were used.
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Table 1. The average parameters of the water in the tank with pikeperch larvae during the experiment. M, mean value; se, standard error of the mean.
Table 1. The average parameters of the water in the tank with pikeperch larvae during the experiment. M, mean value; se, standard error of the mean.
Parameter of WaterM ± sePermissible Range (PR)
Oxygen (O2) concentration, mg/L9.3 ± 0.3≥6.0
Oxygen saturation, %92.6 ± 3.9-
Temperature, °C19.6 ± 2.715 < PR < 26
pH6.8 ± 0.16.5 < PR < 8.5
CO2 concentration, mg/L3.2 ± 0.8<20
Ammonium nitrogen (N), mg/L0.24 ± 0.1<0.40
Nitrites (N), mg/L<0.010<0.020
Nitrates (NO3), mg/L0.89 ± 0.16<40.0
Phosphates (P), mg/L<0.010<0.15
Table 2. Biochemical composition of the zooplankton sampled from Sukhodolskoye Lake (in percentages) and water temperature during the experiment. Three replicates for each probe were used.
Table 2. Biochemical composition of the zooplankton sampled from Sukhodolskoye Lake (in percentages) and water temperature during the experiment. Three replicates for each probe were used.
ParameterProbe 1Probe 2Probe 3Probe 4
Fish larval developmental stage, days post-hatching (dph)391521
Water temperature, °C15.918.521.521.7
Biochemical parameters, %
Dry matter10.64 ± 1.64 a10.82 ± 1.48 a9.43 ± 1.23 b9.03 ± 1.12 b
Protein68.00 ± 2.1168.10 ± 1.9870.50 ± 2.3068.90 ± 1.64
Lipids24.88 ± 3.64 a24.71 ± 3.05 a22.52 ± 2.90 b22.27 ± 2.76 b
Nitrogen-free extract (NFE)3.84 ± 1.743.23 ± 1.614.09 ± 1.343.67 ± 1.29
Ash3.28 ± 0.60 a3.96 ± 0.52 b2.89 ± 0.66 a5.16 ± 1.36 c
a,b,c Values (mean ± SD) in the same row with different letters indicate significant differences (p ≤ 0.05).
Table 3. Fatty acid composition of the lipids in the zooplankton sampled from Sukhodolskoye Lake (in percentages) and water temperature during the experiment. FAs, fatty acids; SFAs, saturated fatty acids; MUFAs, monosaturated fatty acids; UFAs, unsaturated fatty acids. Three replicates for each probe were used.
Table 3. Fatty acid composition of the lipids in the zooplankton sampled from Sukhodolskoye Lake (in percentages) and water temperature during the experiment. FAs, fatty acids; SFAs, saturated fatty acids; MUFAs, monosaturated fatty acids; UFAs, unsaturated fatty acids. Three replicates for each probe were used.
ParameterProbe 1Probe 2Probe 3Probe 4
Fish larval developmental stage, days post-hatching (dph)391521
Water temperature, °C15.918.521.521.7
Fatty acids (FAs), %
12:0-0.41 ± 0.08 a0.46 ± 0.12 a1.27 ± 0.35 b
14:02.95 ± 0.53 a5.68 ± 1.08 b6.91 ± 0.92 b7.94 ± 2.59 c
15:01.39 ± 0.44 a0.85 ± 0.08 b1.18 ± 0.16 b1.86 ± 0.42 a
16:019.64 ± 1.85 a19.25 ± 2.14 a23.75 ± 2.22 b32.68 ± 3.30 c
18:02.93 ± 0.18 a5.23 ± 1.11 b5.65 ± 1.14 b6.41 ± 0.72 b
22:00.32 ± 0.13 a0.61 ± 0.12 b0.38 ± 0.08 a-
23:00.33 ± 0.09 a1.25 ± 0.35 b0.32 ± 0.11 a0.50 ± 0.06 c
16:1 n-70.30 ± 0.04 a0.51 ± 0.11 b0.43 ± 0.09 b0.48 ± 0.09 b
16:1 n-94.16 ± 1.11 a4.29 ± 1.54 a6.22 ± 1.13 b4.70 ± 1.11 a
17:1 n-91.72 ± 0.08 a1.66 ± 0.19 a1.43 ± 0.11 b1.34 ± 0.20 b
18:1 n-75.98 ± 0.92 a9.34 ± 2.59 b,c5.56 ± 1.08 a7.27 ± 0.92 c
18:1 n-95.50 ± 1.08 a,b4.91 ± 1.28 b5.86 ± 1.20 a6.19 ± 0.96 a
20:1 n-70.07 ± 0.01 a-0.10 ± 0.01 a1.25 ± 0.05 b
22:1 n-95.87 ± 1.06 a12.33 ± 0.61 b1.98 ± 1.66 b4.46 ± 0.92 a
18:2 n-6 Linolenic acid (LA)6.59 ± 1.11 a5.18 ± 0.88 a,b4.81 ± 0.64 b3.05 ± 0.30 c
20:2 n-60.11 ± 0.01 a0.17 ± 0.02 a--
20:4 n-6 Arachidonic acid (ARA)21.14 ± 2.89 a4.31 ± 0.70 b3.31 ± 0.53 c1.48 ± 0.93 d
22:2 n-60.14 ± 0.01 a1.55 ± 0.42 b1.22 ± 0.38 b-
18:3 n-3 Alpha-linolenic acid (ALA)5.61 ± 0.72 a7.55 ± 1.14 b8.53 ± 0.92 b6.08 ± 0.84 a
18:4 n-32.87 ± 0.53 a,c4.54 ± 1.08 b3.13 ± 1.02 a,b,c2.07 ± 0.71 c
20:5 n-3 Eicosapentaenoic acid (EPA)4.44 ± 0.72 a1.64 ± 0.55 b3.12 ± 0.53 a2.12 ± 0.14 c
22:5 n-30.39 ± 0.04 a0.37 ± 0.03 a--
22:6 n-3 Docosahexaenoic acid (DHA)0.70 ± 0.13 a2.82 ± 0.20 b1.82 ± 0.22 c1.64 ± 0.16 c
n/d6.23 ± 0.56 a5.76 ± 0.44 a4.64 ± 0.35 b7.20 ± 0.58 c
Σ SFAs27.71 ± 2.84 a33.28 ± 3.12 b38.65 ± 4.42 b50.66 ± 4.88 c
Σ MUFAs23.69 ± 7.29 a33.04 ± 3.09 b30.58 ± 3.13 b25.69 ± 7.04 a
Σ UFAs42.37 ± 3.60 a27.63 ± 2.07 b25.94 ± 1.98 b16.44 ± 1.73 c
n-314.01 ± 1.24 a16.92 ± 1.36 b16.60 ± 1.05 b11.91 ± 0.68 c
n-628.36 ± 1.73 a10.71 ± 0.89 b9.34 ± 0.80 b4.53 ± 0.40 c
EPA + DHA5.14 ± 0.85 a4.46 ± 0.75 a4.94 ± 0.31 a3.76 ± 0.30 b
n-3/n-60.51.61.82.6
ALA/LA0.91.51.82.0
DHA/EPA0.21.70.60.8
a,b,c,d Values (mean ± SD) in the same row with different letters indicate significant differences (p ≤ 0.05). n/d, not defined.
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Lyutikov, A.; Korolev, A.; Trifonov, A.; Zubareva, A.; Nedoluzhko, A. The Diversity and Biochemical Composition of Zooplankton as a Potential Indicator of Dietary Requirements for Pikeperch Larvae (Sander lucioperca). Hydrobiology 2025, 4, 13. https://doi.org/10.3390/hydrobiology4020013

AMA Style

Lyutikov A, Korolev A, Trifonov A, Zubareva A, Nedoluzhko A. The Diversity and Biochemical Composition of Zooplankton as a Potential Indicator of Dietary Requirements for Pikeperch Larvae (Sander lucioperca). Hydrobiology. 2025; 4(2):13. https://doi.org/10.3390/hydrobiology4020013

Chicago/Turabian Style

Lyutikov, Anatoliy, Alexander Korolev, Artem Trifonov, Anastasia Zubareva, and Artem Nedoluzhko. 2025. "The Diversity and Biochemical Composition of Zooplankton as a Potential Indicator of Dietary Requirements for Pikeperch Larvae (Sander lucioperca)" Hydrobiology 4, no. 2: 13. https://doi.org/10.3390/hydrobiology4020013

APA Style

Lyutikov, A., Korolev, A., Trifonov, A., Zubareva, A., & Nedoluzhko, A. (2025). The Diversity and Biochemical Composition of Zooplankton as a Potential Indicator of Dietary Requirements for Pikeperch Larvae (Sander lucioperca). Hydrobiology, 4(2), 13. https://doi.org/10.3390/hydrobiology4020013

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