Abstract
In freshwater ecosystems, the efficiency of transfer of essential substances from phytoplankton to zooplankton, measured as the ratio of the production of these substances in zooplankton to their production in phytoplankton, determines the functioning of higher trophic levels. In addition to carbon, primary producers transfer essential substances, including polyunsaturated fatty acids (PUFAs), nitrogen (N), and phosphorus (P), up the trophic chain. The transfer efficiency of these substances significantly varies in nature depending on environmental factors, which is reflected in the quality of biological resources. The purpose of this review is to analyze the mechanisms regulating the efficiency of the transfer of essential substances from phytoplankton to zooplankton and establish the main factors that may influence the efficiency of their transfer.
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ESSENTIAL SUBSTANCES TRANSFERRED FROM PHYTOPLANKTON TO ZOOPLANKTON
The functioning of trophic chains in freshwater ecosystems depends on the efficiency of transport of essential substances from producers to higher trophic levels. The transfer of carbon up the trophic chain is accompanied by the loss of some portion of the substance due to an incomplete assimilation of the biomass of the previous trophic level by consumers. About 10% of carbon is transferred from one trophic level to the next one (Lindeman, 1942). In addition to carbon (C), physiologically important substances are also transferred through trophic chains; these essential substances include polyunsaturated fatty acids, eicosapentaenoic acid (20:5, omega-3) (EPA) and docosahexaenoic acid (22:6, omega-3) (DHA), N, and P. In nature, a shortage of essential substances in food resources is often observed for zooplankton. This is due to the large difference between their content in food and zooplankton demands (Sterner and Hessen, 1994; Brett and Müller-Navarra, 1997; Twinning et al., 2016). Therefore, it is important to know the efficiency of the transfer of essential substances from phytoplankton to zooplankton, since this determines the quality of zooplankton as a resource for higher trophic levels.
Fatty Acids
Fatty acids are bioactive molecules responsible for many bodily functions. Some of them are used for catabolism and others for physiological processes (Bell and Tocher, 2009; Taipale et al., 2011). In particular, PUFAs included in phospholipids are used as a building material for cell membranes. Planktonic communities are the main suppliers of essential PUFAs up the trophic chain, in particular, to fish. DHA is a priority acid. This molecule is contained in the membranes of nerve tissue cells and is critical for reproductive functions in fish (Izquierdo et al., 2001). Its deficiency can lead to a loss of vision (Bell et al., 1995). EPA is involved in the production of biologically active hormone-like substances, namely, eicosanoids (Heckmann et at., 2008; Schmitz and Ecker, 2008). Eicosanoids serve to regulate the cardiovascular system, blood clotting, and immune response in fish. They can also be used to synthesize DHA (Jardine et al., 2020). It has been repeatedly shown that the deficiency of EPA limits the growth and reproduction of daphnids (Martin-Creuzburg et al., 2010; Sperfeld and Wacker, 2011).
Nitrogen and Phosphorus
Nitrogen and phosphorus determine the physiology of consumers (Frost et al., 2005; Wagner et al., 2013). Stoichiometric ratios between C, N, and P are important for consumers. Inconsistencies of the stoichiometric C : N : P ratios in food resources to the physiological demands of zooplankton may affect the synthesis of lipids, proteins, and nucleic acids (Wagner et al., 2015). These changes in metabolism entail a decrease in the rates of individual growth, reproduction, and survival (Sterner, 1993; Frost et al., 2005). The C : P ratio in nature often exceeds threshold values, i.e., the level at which the production of crustaceans begins to be limited by phosphorus.
The purpose of this review is to analyze the mechanisms regulating the efficiency of transfer of essential substances from phytoplankton to zooplankton and establish the main factors that may influence the efficiency of their transfer. The transfer efficiency of essential substances depends on their content (i.e., their weight per unit of carbon) and production in both phytoplankton and zooplankton.
CONTENT OF ESSENTIAL SUBSTANCES IN PHYTOPLANKTON
Fatty Acids
The fatty acid profile of phytoplankton varies widely and can depend both on the taxonomic structure and on environmental conditions. M.I. Gladyshev et al. (2007) showed that changes in the indices of food quality in the Bugach eutrophic reservoir, measured in terms of the content of essential substances and stoichiometric ratios, were more correlated with the dynamics of the taxonomic structure of phytoplankton than with the environmental conditions. In particular, the cyanobacterium Anabaenaflos-aquae (Lyngb.) Breb. contained only α-linolenic acid (18 : 3, omega-3) (ALA), the diatom Stephanodiscus spp. contained mainly EPA, and the dinoflagellate Peridinium sp. was especially rich in DHA. The data of (Gladyshev et al., 2007) indicate that different algal species have a specific structure of the elemental and PUFA compositions. Therefore, it can be concluded that the quality of food resources largely depends on the taxonomic composition of phytoplankton.
Other researchers have also paid attention to the species specificity of the fatty acid profile in algae (Strandberg et al., 2015). It was shown that dinophytes are characterized by a high content of DHA (Ahlgren et al., 1997; Sushchik et al., 2004; Gutseit et al., 2007). Diatoms are characterized by a high EPA concentration, which can reach 30% of total FAs (Caramujo et al., 2008; Breuer et al., 2013; Bellou et al., 2014), while the content of EPA in cryptophytes and dinophytes does not exceed 10% (Ahlgren et al., 1992, Taipale et al., 2013). Cryptophytes are characterized by stearic acid (STD) (18:4, omega-3) (Ahlgren et al., 1992). Cyanobacteria cannot synthesize PUFAs with a chain length of more than 18 carbon atoms; however, they synthesize PUFAs with 18 carbon atoms (Tocher et al., 1998). In addition, the content of PUFAs can also significantly vary within the same taxonomic group. N.N. Sushchik et al. (2004) showed that two diatom species significantly differed in EPA content. In particular, the concentration of EPA was insignificant in diatoms Cyclotella atomus Hust. and C. meneghiniana Kutz, while Stephanodiscus hantzschii Grun. and S. minutulus (Kutz.) Cleve & Moller contributed greatly to the total EPA content in seston. Among cyanobacteria, two species, Anabaena flos-aquae Bréb. ex Born. & Flauh. and Planktothrix agardhii (Gom.) Anagn. & Kom., showed a high correlation with α-linolenic acid (ALA), while this FA was absent in two other species, Aphanizomenon flos-aquae Ralf. ex. Born. & Flah. and Microcystis aeruginosa (Kütz.) Kütz. O. Kormilets (2019) noted a high variability in the FA content depending on the species identity and habitat. For example, freshwater chrysophytes synthesize large amounts of fatty acids of the n-3 and n-6 families, while marine species of Chrysophyceae are poor in fatty acids of the n-6 family.
Species-specific differences in the composition of FAs in algae are determined by the fact that different taxa differ in their sets of enzymes (desaturases); therefore, they synthesize different FAs (Gugger et al., 2002; Dijkman and Kromkamp, 2006; Kelly and Scheibling, 2012; Galloway and Winder, 2015). The availability of a certain set of desaturases is determined by the genotype. Although the differences in the composition of FAs and stoichiometric ratios are great between the taxa, these parameters may also vary depending on environmental conditions.
The amount of PUFAs decreases under stress conditions. For instance, an increase in temperature leads to a decrease in the content of PUFAs both in cyanobacteria and in algae (Sushchik et al., 2003). Global climate warming may lead to a decrease in the production of PUFAs as a result of the capability of algal cells for homeoviscose adaptation, i.e., their ability to maintain a constant viscosity of cell membranes by reducing the proportion of PUFAs in lipids when the environmental temperature increases (Guschina and Harwood, 2006; Hixson and Arts, 2016). This was confirmed by Hixson and Arts (2016), who revealed a significant decrease in the proportion of long-chain omega-3 PUFAs and a simultaneous increase in the proportions of omega-6 FAs and saturated FAs in the total amount of FAs in algal cells with an increase in water temperature. Based on linear regression models, the authors predicted that an increase in water temperature by 2.5°C would lead to a decrease in the global production of EPA and DHA by 8.2 and 27.8%, respectively. On the contrary, the amount of PUFAs is expected to increase in cell membranes under the effect of low temperatures, which is determined by the synthesis of the corresponding desaturases in this case (Guschina and Harwood, 2006). In addition, temperature increase can involve the replacement of the main producers of PUFAs (diatoms, cryptophytes, and dinophytes) by cyanobacteria of poor quality, which do not produce EPA and DHA (Caramujo et al., 2008). Therefore, the decrease in PUFAs with an increase in temperature may be caused by two factors: a change in the taxonomic composition and the suppression of the synthesis of desaturases. In addition to temperature, the desaturase activity may be induced by the effect of high oxygen concentrations in the water. An increase in temperature leads to a decrease in the concentration of dissolved oxygen, which causes an even greater suppression of the activity of desaturases. These two factors can reinforce each other (Strandberg et al., 2015).
Stoichiometric Ratios
Redfield (1934) noted for the first time that the average N : P ratio for marine algae was 16 : 1. Later, many researchers showed that this ratio was far from constant and depended on the species identity and environmental conditions (Klausmeier et al., 2004). For instance, it was shown that the N : P ratio in biomass varied from 15 to 42 for Chlorella vulgaris Beijer, while it was 7–32 for Scenedesmus obliquus (Turp.) Kütz. (Beuckels et al., 2015). The content of N and P in algal cells varies over a wide range (Sterner and Hessen, 1994). Thus, the content of P can vary from 0.03 to more than 3% of the dry weight and that of N from 3 to 12% in algal cells (Reynolds, 2006).
Reynolds (2006) noted that the growth of phytoplankton was possibly regulated by the co-limitation of N and P, instead of by either of them individually. His study showed that the growth of phytoplankton was limited at concentrations of dissolved inorganic P below 3–10 µg/L and dissolved N below 100–130 µg/L. These are threshold concentrations of nutrients, below which the growth of phytoplankton slows. Different algal species have their own species-specific demands and, consequently, their own threshold concentrations. This was confirmed by A.P. Levich and N.G. Bulgakov (Levich and Bulgakov, 1992), who showed that the taxonomic and size structures of phytoplankton changed in dependence on the N : P ratio. High N : P values (20–50) were favorable for the development of protococcal algae, while the decrease in the N : P ratio to 5–10 led to the dominance of cyanobacteria in the community (Bulgakov and Levich, 1995). The authors concluded that the ratio of concentrations of nutrients in the environment should be recognized as an independent abiotic factor that regulates the taxonomic and size structure of phytoplankton, thereby changing its quality as a food resource for zooplankton.
The relationship between N and P can be explained by the fact that the assimilation of P by algae depends on the concentration of dissolved inorganic N, while the assimilation of N does not depend on the concentration of inorganic P (Beuckels et al., 2015), which is explained by different functions of N and P in cellular metabolism (Loladze and Elser, 2011). In microalgae, N is required mainly for protein synthesis. The deficiency in N causes a reduction of protein synthesis, which leads to a decrease in the number of ribosomes and ribosomal RNAs. Since most of the P content in a cell is stored in ribosomal RNA, a decrease in the number of ribosomes leads to a decrease in the demand for P (Beuckels et al., 2015). Therefore, the reduction of N assimilation also entails the reduction of assimilation of P.
The content of N and P in phytoplankton increases with an increase in the concentration of inorganic compounds of these elements in the environment (Sterner and Elser, 2002; Beuckels et al., 2015). In addition, when the concentrations of N and P are excessive, algae can store nutrients for future use (Eixler et al., 2006). Diatoms accumulate nitrates in the central vacuole (Coppens et al., 2014). Some species can accumulate P to 3% of dry weight in the form of polyphosphate granules (Eixler et al., 2006; Powell et al., 2009).
In addition, stoichiometric ratios can depend on cell size (Finkel et al., 2010), since the cell size influences both the absorption of elements and their assimilation (Schulhof et al., 2019). Small cells assimilate nutrients under conditions of their deficiency more efficiently than large cells, since they have a higher ratio of the surface area to the volume and a thinner diffuse boundary layer. However, large cells can store more nutrients. Therefore, small algae gain a competitive advantage under conditions of low trophic level, while large algae are more competitive in an environment with high trophic level and rapidly changing concentrations of nutrients (Edwards et al., 2011; Cloern, 2018). Schulhof et al. (2019) revealed that C : P of the fine-fraction of algae (<30 µm) was lower than that of the coarse-fraction (>30 µm) at low trophic level. C : P in the coarse-fraction of algae decreased in algae with an increase in trophic level, while C : P of the fine-fraction of algae did not change, which indicated a higher sensitivity of large cells to the concentration of inorganic phosphorus in the medium.
It should be noted that the content of nutrients in algae depends on temperature (Schulhof et al., 2019). Climate warming sometimes leads to a decrease in the C : P and N : P ratios in algae, which is explained by an increase in the concentrations of nutrients in the environment as a result of an increase in the rate of their regeneration by consumers or microbial communities with an increase in temperature (Velthuis et al., 2017). Warming can also have opposite effects; i.e., it can increase N : P in phytoplankton, which is explained by an increase in the rate of protein biosynthesis and a decrease in the number of ribosomes (Toseland et al., 2013). Therefore, stoichiometric ratios in phytoplankton depend not only on taxonomic identity, but also on abiotic factors.
CONTENT OF ESSENTIAL SUBSTANCES IN ZOOPLANKTON
Fatty Acids
Zooplankton can synthesize only some PUFAs, while the bulk of PUFAs should be consumed by zooplankton together with food. For instance, daphnids synthesize only 0.5% of EPA from lipoic acid (Twining et al., 2016). Therefore, the composition of PUFAs in consumers may depend on their content in food resources. Hessen and Leu (2006) studied the composition of fatty acids in zooplankton and seston. The results of their study clearly showed that the fatty acid profile in daphnids differed between lakes with different taxonomic structures of phytoplankton; the composition of FAs was correlated with the taxonomic composition of phytoplankton. However, the average content of EPA was 1.7 times higher in daphnids than in phytoplankton, while the content of DHA was 0.08 times lower in daphnids than in seston. Therefore, daphnids can regulate the content of PUFAs. Here, it should be noted that cladocerans require more EPA and less DHA than copepods (Desvilettes et al., 1997a; Weers et al., 1997; Ballantyne et al., 2003; Brett et al., 2009; Ravet et al., 2010; Gladyshev et al., 2015). Therefore, the content of EPA is high and that of DHA is low in zooplankton when it is dominated by daphnids.
It has been repeatedly noted that zooplankton exhibit homeostasis (Hessen and Leu, 2006); i.e., it can maintain a relatively constant elemental and biochemical composition. Therefore, mechanisms regulating the content of essential substances in the body might develop in zooplankton in the process of evolution. There are different mechanisms for increasing the content of these substances in zooplankton.
Essential FAs, i.e., FAs that are not synthesized de novo by zooplankton, are not often consumed in the required amount; however, they can accumulate in the tissues of invertebrates and even exceed their content in food resources. Taipale et al. (2011) studied the patterns of PUFA regulation in cladocerans. When high-quality food (Cryptomonas ozolinii Skuja) for daphnids was replaced by lower quality food (Scenedesmus obliquus), they began to selectively retain EPA and arachidonic acid (20 : 4, omega-6) (ARA), i.e., more essential FAs. The isotopic method based on δ13C showed that EPA and ARA could be synthesized in the body of Daphnia magna (Straus, 1820) from FA precursors received with food. Molecules of some FAs are converted into the molecules of other FAs through the elongation of the carbon chain or the formation of unsaturated bonds as a result of desaturation (Dalsgaard et al., 2003; Brett et al., 2009). The synthesis involves enzymes increasing the length of the carbon chain (elongases) and desaturases (Gladyshev, 2012). Therefore, daphnids can increase the content of essential FAs due to their biosynthesis under conditions of poor quality of food resources.
Different taxa differently regulate the composition and content of PUFAs. For instance, cyclops accumulate predominantly DHA (Desvilettes et al., 1997b), diaptoms convert EPA to DHA (Ravet et al., 2010), and cladocerans biosynthesize EPA and ARA from their precursors (Kainz et al., 2004, Ravet et al., 2010; Taipale et al., 2011). Among all FAs, DHA is characterized by the highest coefficient of accumulation in heterotrophs, since this acid is not catabolized for energy production, unlike less essential FAs (Jardine et al., 2020). With respect to its properties, it is not suitable as a substrate for β-oxidation. It was shown that the content of DHA was higher in zooplankton than in seston to a greater extent than other FAs, including EPA (Sakharova et al., 2021; Feneva et al., 2021). It should be noted that ALA, which can be synthesized by cyanobacteria, can be converted into EPA in crustaceans. Therefore, nontoxic cyanobacteria can support the growth of daphnids.
Other mechanisms for increasing the content of PUFAs in zooplankton are also possible. The selectivity of consumption of more essential food particles is typical mainly for copepods (De Mott, 1986). It is known that the range of food particles consumed by filter-feeding crustaceans is limited only by their size (Sommer and Sommer, 2006). They cannot selectively filter higher quality food particles; however, phytoplankton is vertically distributed so that the most essential algae (cryptophytes) are often dominant in the metalimnion, where filter-feeding crustaceans can also concentrate (Burns et al., 2011). Cladocerans can also differently metabolize food particles; as a result, the diet of filter-feeding crustaceans can be selective (Feniova et al., 2018). The selective feeding of zooplankton is confirmed by data on the isotopic composition (δ13C) of zooplankton and phytoplankton from oligotrophic, mesotrophic, eutrophic, and dystrophic lakes (Taipale et al., 2016). Based on an analysis of stable isotopes, Taipale et al. showed that the δ13C of crustaceans was correlated with the δ13C of individual algal taxa, rather than with δ13C of total phytoplankton. Selective feeding was also noted by Gladyshev et al. under field and experimental conditions (Gladyshev et al., 1999); they showed that Ceriodaphnia quadrangula (O.F. Müller, 1785) mainly consumed Cryptomonas erosa Ehr., although it was not the only food resource in the environment.
Stoichiometric Ratios
The stoichiometric N : C and P : C ratios in zooplankton species vary within a narrow range; i.e., these parameters are more stable in zooplankton than in phytoplankton (Sterner, 1989; Hessen, 1990; Andersen and Hessen, 1991; Dubovskaya, 2009). Therefore, it can be stated that zooplankton species are characterized by the homeostasis of elemental ratios (Sterner, 1990; Dubovskaya, 2009). In freshwater zooplankton, the C : N : P atomic ratios are species-specific and vary within a narrow range. In particular, according to Andersen and Hessen (1991), the average value of this ratio is 212 : 39 : 1 in Acanthodiaptomus denticornis (Wierzejski, 1887), while it is 85 : 14 : 1 in Daphnia longispina (O.F. Müller, 1776). They also showed that the zooplankton species differed less in the content of nitrogen (N : C) than in the content of phosphorus (P : C). And, the content of P increased in the series Acanthodiaptomus denticornis, Heterocope saliens (Lilljeborg, 1863), Bosmina longispina (Leydig, 1860), Holopedium gibberum (Zaddach, 1855), Diaphanosoma brachyurum (Liévin, 1848), and Daphnia longispina.
It should be added that large and small cladoceran species (the family Daphniidae) differ in stoichiometric ratios. Namely, large daphnids have a lower C : P value and are therefore more sensitive to phosphorus limitation than small species of this family, such as Ceriodaphnia sp., which, on the contrary, are more sensitive to nitrogen limitation (Elser et al., 1996, 2000; Iwabuchi and Urabe, 2010). Therefore, the content of these elements in cladocerans is mainly determined by their taxonomic composition.
Similarly to PUFAs, the content of N and P is often higher in zooplankton than in food resources (Urabe and Watanabe, 1992). When the content of N and P is deficient in food, crustaceans can concentrate these elements in their tissues to satisfy their needs. M. Karpowicz et al. (2019) revealed differences in the C : P and C : N ratios between phytoplankton and zooplankton in experimental mesocosms. For instance, the C : P ratio was 2–3 times lower in zooplankton than in seston. The increase in the content of P in zooplankton was accompanied by a decrease in the concentration of phosphates in the water. Therefore, the authors concluded that zooplankton could accumulate P, thereby serving as some kind of phosphorus sink. It should be noted that the level of P accumulation is higher in the tissues of cladocerans than in the tissues of copepods. In particular, the content of P in herbivorous cladocerans (Bosmina, Diaphanosoma, Holopedium, and, in particular, Daphnia) is up to 2% of dry weight, while its content in freshwater copepods varies from 0.4 to 0.8% of dry weight (Sterner and Hessen, 1994).
Stoichiometric ratios can be influenced by abiotic factors. An increase in temperature leads to a decrease in C : P as a result of a decrease in C reserves in crustacean tissues, which involves changes in P metabolism (Prater et al., 2018). In addition to temperature, the animal metabolism can also be influenced by other factors, such as light, CO2, predation, and parasitism (Prater et al., 2018). Therefore, the stoichiometry of zooplankton can vary throughout the season. The effects of abiotic and biotic factors on animal metabolism explains frequently observed differences in the biochemical and elemental compositions of zooplankton from different habitats. However, these differences are less significant than those between different taxa.
There are different mechanisms for regulating the relative constancy of stoichiometric elemental ratios in zooplankton, e.g., by increasing the feeding rate or retaining N or P in tissues when the content of these elements is deficient (Sterner and Elser, 2002). Excess of N or P can be excreted together with waste products (Sterner and Hessen, 1994; Sterner and Elser, 2002). According to the concept of threshold elemental ratios (TERs), the element which is the most deficient is assimilated with greater efficiency. In nature, the content of P is often deficient for zooplankton. Therefore, P is often assimilated with 100% efficiency, while C is assimilated with 60% efficiency; in addition, the efficiency of C assimilation decreases linearly with an increase in C : P (Hessen et al., 2013). The release of P may completely stop if the C : P ratio begins to exceed 320–430 in food resources, i.e., at a low content of P (Olsen et al., 1986; Karpowicz et al., 2019). Another way to regulate stoichiometric ratios is the removal of excess of C during respiration or its release together with organic waste products. In addition, excess of C can either not be assimilated in the gut or accumulate in the form of lipids. Therefore, zooplankton can increase the content of essential substances in its tissues by regulating the rate of food consumption and metabolic and physiological processes.
PRODUCTION OF ESSENTIAL SUBSTANCES IN PHYTOPLANKTON AND ZOOPLANKTON
Since the efficiency of transfer of essential substances from phytoplankton to zooplankton is determined as the ratio of their production in zooplankton to their production in phytoplankton, the higher the production of essential substances in zooplankton, the higher the efficiency of their transfer. The amount of C rarely limits the growth of crustaceans in freshwater ecosystems except for oligotrophic water bodies (White, 1993). Therefore, the production of zooplankton under mesotrophic and eutrophic conditions can be limited by PUFAs (Müller-Navarra et al., 2000, 2004; Persson et al., 2007) and P and N (Prater et al., 2018).
Prater et al. (2018) believe that stoichiometric ratios may influence the production of daphnids. Field studies in two lakes in Ontario (Canada) with different phosphorus loads showed that the stoichiometric ratios in food resources influenced the production of daphnids in the lake with the low phosphorus load (Prater et al., 2018). The production of daphnids in this lake increased with a decrease in the C : P ratio in the food resources of daphnids. In the lake with the high phosphorus load and low C : P ratio in phytoplankton, the production of daphnids was not correlated with the C : P ratio in food resources. Therefore, stoichiometric ratios can influence the production of daphnids only in the range of a low P content in food resources, i.e., in lakes with a low trophic level. As a result, control of the production of daphnids would be shifted to physical factors, e.g., temperature, or biochemistry, including FAs, with increase of trophic level. Therefore, one should expect limitation by nutrients under oligotrophic conditions, while the production under eutrophic conditions will be regulated by the biochemical composition of resources. Sterner (1997) also noted that factors regulating zooplankton communities replaced each other depending on environmental conditions. If daphnids are starving (i.e., if they lack C), their growth is limited by C; if C does not limit the growth of daphnids, their production begins to depend on food quality.
Prater et al. (2018) showed that stoichiometric ratios in phytoplankton influenced the production of zooplankton in combination with temperature. In Wolf Lake (Ontario, Canada) with a low phosphorus load, the production of planktonic crustaceans was correlated both with food quality (C : P) and with temperature. The highest production of zooplankton was observed at a low C : P ratio and moderate temperatures. Therefore, the effect of temperature can modify the mechanisms of influence of stoichiometric ratios on the production of zooplankton, which may lead to seasonal changes in their production.
Hessen et al. (2013) noted that the difference between phytoplankton and zooplankton was greater in the P content than in the N content. This may be determined by the fact that the C : P ratio varies over a wider range than C : N in phytoplankton and that P directly influences the growth rate of zooplanktonic organisms (Hessen et al., 2013). Different representatives of zooplankton respond differently to P and N limitation. In particular, it has been shown that the biomass of daphnids, which contains more P in their tissues, is significantly correlated with the concentration of mineral P (Andersen and Hessen, 1991; Hesen, 1992). Copepods, which are characterized by a higher N content, are correlated better with the concentration of mineral N. Therefore, when the amount of one of the elements (N or P) is limited, species that are less vulnerable to its shortage gain the advantage. The shift between N or P limitation, which is often observed in nature, may lead to changes in the species structure of zooplankton, which, in turn, will involve changes in the secondary production and efficiency of transfer of substances from phytoplankton to zooplankton (Sterner, 1993).
The limitation of the secondary production of PUFAs, which they receive with food, is explained by a huge discrepancy in nature between the demands of heterotrophs in these substances and their content in food (Twining et al., 2016). It has been shown that a high content of EPA, DHA, and ARA in food would increase the production of zooplankton (Brett and Müller-Navarra, 1997; Sargent et al., 1999; Parrish et al., 2007). For instance, Müller-Navarra et al. (2000) clearly demonstrated that the production of daphnids in a hypereutrophic pond (Davis Pond, California, United States) depended on the content of PUFAs in phytoplankton. Their study showed that the production of daphnids was very low in summer, and the clutch size varied from 0 to 0.5 eggs per clutch despite the high phytoplankton biomass (3.9–9.4 mg C L–1). Cyanobacteria with a negligibly low content of EPA prevailed during that time. In winter, when diatoms with a high content of EPA began to prevail in phytoplankton, the production of daphnids and their average clutch size increased (9.1–17.0 eggs per clutch) compared to the summer values, although the phytoplankton biomass decreased more than two times (up to 1.7–3.8 mg C L–1). The authors explained the absence of the relationship between the biomasses of phytoplankton and zooplankton by the fact that the production of the consumers depended on the quality of food rather than on its amount. This conclusion is also confirmed by the fact that the highest correlation was found between the production of daphnids and content of EPA in seston. Contrary to expectations, chlorophyll a did not influence the production of daphnids. Therefore, the authors concluded that the content of EPA in phytoplankton in eutrophic water bodies may be the main factor controlling the secondary production.
It should be noted that small and large zooplankton species can respond differently to the same levels of food quantity and quality. Under experimental conditions, it was shown that the growth rate of the small species Ceriodaphnia pulchella (Sars, 1862) was correlated with the amount of food resources, while the production of large daphnids (Daphnia magna (Straus, 1820) and Daphnia pulicaria (Forbes, 1893)) responded more strongly to EPA shortage (Feniova et al., 2019). Therefore, small and large zooplankton species have different survival strategies under unfavorable food conditions, which leads to a shift in dominance between small and large species depending on environmental conditions.
EFFICIENCY OF TRANSFER OF ESSENTIAL SUBSTANCES FROM PHYTOPLANKTON TO ZOOPLANKTON
An increase in the content of essential substances in zooplankton relative to that in the food provides more efficient transfer of these substances from phytoplankton to zooplankton. It can be assumed that, the higher the content of essential substances in zooplankton relative to that in their resources, the higher their production and, consequently, the higher the efficiency of transfer of these substances from phytoplankton to zooplankton. The results of the work of Gladyshev et al. (2011) on flows of total organic carbon and essential n-3 PUFAs and FAs in the Bugach eutrophic reservoir showed that different substances were transferred from phytoplankton to zooplankton with different efficiencies. In particular, the efficiency of transfer of PUFAs from phytoplankton to zooplankton was two times higher than that of organic carbon. However, C16-PUFA, which serves only as an energy source for animals, were transferred less efficiently than total organic carbon. In zooplankton, C16-PUFA undergoes mitochondrial β-oxidation more often than essential PUFAs (Leonard et al., 2004). Therefore, less essential FAs are generally used for catabolic processes, while more essential acids are stored. Thus, the content of PUFAs can increase with each level of the trophic chain and, as a result, the trophic pyramid of production of essential PUFAs will expand upwards rather than getting narrower, as in the case of carbon (Gladyshev et al., 2011).
The trophic status and depth of a water body can influence the efficiency of transfer of substances from phytoplankton to zooplankton. Based on the studies of 56 lake with different depths, along the trophic gradient (ultraoligotrophic, oligotrophic, mesotrophic, and eutrophic lakes), the efficiency of transfer of matter from phytoplankton to zooplankton significantly decreased both in shallow and deep lakes (Lacroix et al., 1999). However, patterns of the effect of the trophic status on the efficiency of material transfer differed between shallow and deep lakes. This might be caused, at least partially, by the use of alternative sources of food resources by zooplankton in shallow lakes (benthic and periphytic taxa in addition to planktonic algae). It is likely that the differences in the efficiency of transfer of matter from phytoplankton to zooplankton in water bodies with different trophic levels are attributed to differences in the fish pressure on zooplankton. It was shown that fish pressure on zooplankton enhanced with an increase in trophic level (Downing et al., 1990).
The efficiency of transfer of essential substances from phytoplankton to zooplankton can be influenced by biotic factors. Dreissena polymorpha (Pallas, 1771) is a strong biotic factor influencing planktonic communities. The zebra mussel can significantly reduce the quantity of phytoplankton by its filtration activity (Vanni, 2002; Conroy and Culver, 2005; Conroy et al., 2005). It is capable of selective feeding by rejecting low-quality algae; in particular, it can selectively consume seston with a high content of EPA, i.e., diatoms (Makhutova et al., 2013). The zebra mussel can induce the “blooms” of cyanobacteria of Microcystis species under conditions of low trophic levels as a result of the excretion of nutrients (Raikow et al., 2004; Knoll et al., 2008; Sarnelle et al., 2012; Vanderploeg et al., 2017); on the contrary, under conditions of high trophic levels, the mollusks reduced the abundance of cyanobacteria as a result of their consumption (Waajen et al., 2016). Experimental studies showed that the zebra mussel increased the concentration of inorganic P in water, which leads to an increase in its content in algae, thereby facilitating the development of large daphnids (Feniova et al., 2015, 2018). It has been shown that the zebra mussel promoted the development of inedible filamentous green algae (Feniova et al., 2020), which suppressed edible phytoplankton fraction. As a result, it can significantly influence the development of phytoplankton and, consequently, its production and the efficiency of transfer of substances from phytoplankton to zooplankton.
Manipulation with the presence/absence of the zebra mussel in the experiments made it possible to assess its influence on the efficiency of transfer of C, N, P, EPA, DHA, and total FAs from phytoplankton to zooplankton (Sakharova et al., 2021). The zebra mussel reduced the efficiency of transfer of all these substances compared to the control. However, it differently influenced the efficiency of transfer of individual essential substances. In particular, it reduced the transfer efficiency by 6 times for C, by 3 times for EPA, by 4 times for DHA, by 3 times for total fatty acids, by 6 times for N, and by 7 times for P compared to the control (Sakharova et al., 2021). This effect might be related to the negative effect of the zebra mussel on the biomass and production of zooplankton as a result of its competition with zooplankton species for food resources, and to the shift in the structure of phytoplankton towards the filamentous green algae inaccessible to zooplankton.
Another biotic factor influencing the transfer of matter and energy from phytoplankton to zooplankton is fish. Planktivorous fish can change the structure of zooplankton by selectively grazing larger individuals (Gliwicz, 2003) or slow-swimming cladocerans, which, unlike copepods, cannot actively avoid fish attacks (Bohl, 1982; Okun and Mehner, 2005). Fish can also influence the structure of phytoplankton communities by excreting waste products into the water, thereby changing the chemical composition of substances available for phytoplankton (Happey-Wood and Pentecost, 1981; Lin and Schelske, 1981; Brabrand et al., 1984). As a result, fish can cause changes in the production of phytoplankton and zooplankton and, consequently, affect the efficiency of transfer of essential substances from phytoplankton to zooplankton.
Since fish consume zooplankton and significantly reduce its biomass, their effect on zooplankton production should be assessed in terms of zooplankton potential production, i.e., the P/B ratio (production per unit of biomass). I.Yu. Fenieva et al. (2021) determined the effects of fish on the ratio of P/B in zooplankton to that in phytoplankton, which reflects the efficiency of matter transfer per biomass unit. It was found that fish increased the efficiency of C transfer by two times, P by 12.4 times, N by 2.5 times, EPA by 12.4 times, DHA by 7.4, and total FAs by 10 times compared to those in the control. Therefore, zooplankton use food resources more efficiently in the presence of fish likely due to reduction of competition between zooplankton species.
CONCLUSIONS
The efficiency of the transfer of substances from phytoplankton to zooplankton is controlled by many factors, including food quality (expressed by the content of PUFAs and stoichiometric ratios), the trophic status of the water body, the taxonomic composition of zooplankton and phytoplankton, temperature, etc. However, the analysis of different studies shows that the level of the effects of factors is not as important as the balance between effects of multiple factors. Therefore, ecological stoichiometry as a separate area has appeared in ecology. Sterner and Elser (2002) defined ecological stoichiometry as a science that studies the balance between different chemicals involved in ecological processes. The limiting factor is similar to the element that is insufficient to maintain the balance, like in Liebig’s law of minimum. If there is an imbalance between any of the variables regulating plankton, this will affect their production and the efficiency of transfer of substances from producers up the trophic chain.
REFERENCES
Ahlgren, G., Goedkoop, W., Markensten, H., Sonesten, L., and Boberg, M., Seasonal variation in food quality for pelagic and benthic invertebrates in Lake Erken—the role of fatty acids, Freshwater Biol., 1997, vol. 38, no. 3, pp. 555–570. https://doi.org/10.1046/j.1365-2427.1997.00219.x
Ahlgren, G., Gustafsson, I.-B., and Boberg, M., Fatty acid content and chemical composition of freshwater microalgae, J. Phycol., 1992, vol. 28, no. 1, pp. 37–50. https://doi.org/10.1111/j.0022-3646.1992.00037.x
Andersen, T. and Hessen, D.O., Carbon, nitrogen, and phosphorus content of freshwater zooplankton, Limnol. Oceanogr., 1991, vol. 36, no. 4, pp. 807–814. https://doi.org/10.4319/lo.1991.36.4.0807
Ballantyne, A.P., Brett, M.P., and Schindler, D.E., The importance of dietary phosphorus and highly unsaturated fatty acids for sockeye (Oncorhynchus nerka) growth in lake Washington—a bioenergetic approach, Can. J. Fish. Aquat. Sci., 2003, vol. 60, pp. 12–22. https://doi.org/10.1139/f02-166
Bell, M.V. and Tocher, D.R., Biosynthesis of polyunsaturated fatty acids in aquatic ecosystems: general pathways and new directions, Lipids in Aquatic Ecosystems, New-York: Springer-Verlag, 2009, pp. 211–236.
Bell, M.V., Batty, R.S., Dick, J.R., Fretwell, K., Navarro, J.C., and Sargent, J.R., Dietary deficiency of docosahexaenoic acid impairs vision at low light intensities in juvenile herring (Clupea harengus L.), Lipids, 1995, vol. 30, pp. 443–449.
Bellou, S., Baeshen, M.N., Elazzazy, A.M., Aggeli, D., Sayegh, F., and Aggelis, G., Microalgal lipids biochemistry and biotechnological perspectives, Biotechnol. Adv., 2014, vol. 32, no. 8, pp. 1476–1493. https://doi.org/10.1016/j.biotechadv.2014.10.003
Beuckels, A., Smolders, E., and Muylaert, K., Nitrogen availability influences phosphorus removal in microalgae-based wastewater treatment, Water Res., 2015, vol. 77, pp. 98–106. https://doi.org/10.1016/j.watres.2015.03.018
Bohl, E., Food supply and prey selection in planktivorous cyprinidae, Oecologia, 1982, vol. 53, pp. 134–138.
Brabrand, A., Faafeng, B., Källqvist, T., and Nilssen, P.J., Can iron defecation from fish influence phytoplankton production and biomass in eutrophic lakes?, Limnol. Oceanogr., 1984, vol. 29, no. 6, pp. 1330−1334. https://doi.org/10.4319/lo.1984.29.6.1330
Brett, M.T. and Müller-Navarra, D.C., The role of highly unsaturated fatty acids in aquatic foodweb processes, Freshwater Biol., 1997, vol. 38, no. 3, pp. 483–500. https://doi.org/10.1046/j.1365-2427.1997.00220.x
Brett, M.T., Müller-Navarra, D.C., and Persson, J., Crustacean zooplankton fatty acid composition, in Lipids in Aquatic Ecosystems, New-York: Springer-Verlag, 2009, pp. 115–146.
Breuer, G., Evers, W.A.C., de Vree, J.H., Kleinegris, D.M.M., Martens, D.E., Wijffels, R.H., and Lamers, P.P., Analysis of fatty acid content and composition in microalgae, JoVE, 2013, vol. 80, art. ID e50628. https://doi.org/10.3791/50628
Bulgakov, N.G. and Levich, A.P., Biogenic elements in the environment and phytoplankton: the ratio of nitrogen and phosphorus as an independent factor in regulating the structure of algocenosis, Usp. Sovrem. Biol., 1995, vol. 15, no. 1, pp. 13–23.
Burns, C.W., Brett, M.T., and Schallenberg, M.A., A comparison of the trophic transfer of fatty acids in freshwater plankton by cladocerans and calanoid copepods, Freshwater Biol., 2011, vol. 56, no. 5, pp. 889–903. https://doi.org/10.1111/j.1365-2427.2010.02534.x
Caramujo, M.-J., Boschker, H.T.S., and Admiraal, W., Fatty acid profiles of algae mark the development and composition of harpacticoid copepods, Freshwater Bio-l., 2008, vol. 53, no. 1, pp. 77–90. https://doi.org/10.1111/j.1365-2427.2007.01868.x
Cloern, J.E., Why large cells dominate estuarine phytoplankton, Limnol. Oceanogr., 2018, vol. 63, no. S1, pp. S392–S409. https://doi.org/10.1002/lno.10749
Conroy, J.D. and Culver, D.A., Do dreissenids mussels affect Lake Erie ecosystem stability processes?, Am. Midl. Nat., 2005, vol. 153, no. 1, pp. 20–32. https://doi.org/10.1674/0003-0031(2005)153[0020:DDMALE]2.0.CO;2
Conroy, J.D., Kane, D.D., Dolan, D.M., Edwards, W.J., Charlton, M.N., and Culver, D.A., Temporal trends in Lake Erie plankton biomass: roles of external phosphorus loading and dreissenid mussels, J. Great Lakes Res., 2005, vol. 31, pp. 89–110. https://doi.org/10.1016/S0380-1330(05)70307-5
Coppens, J., Decostere, B., Van Hulle, S., Nopens, I., Vlaeminck, S.E., De Gelder, L., and Boon, N., Kinetic exploration of nitrate-accumulating microalgae for nutrient recovery, Appl. Microbiol. Biotechnol., 2014, vol. 98, pp. 8377–8387.
Dalsgaard, J., John, M.S., Kattner, G., Müller-Navarra, D., and Hagen, W., Fatty acid trophic markers in the pelagic marine environment, Adv. Mar. Biol., 2003, vol. 46, pp. 225–340. https://doi.org/10.1016/S0065-2881(03)46005-7
De Mott, W.R., The role of taste in food selection by freshwater zooplankton, Oecologia, 1986, vol. 69, pp. 334–340.
Desvilettes, C., Bourdier, G., Amblard, C., and Barth, B., Use of fatty acids for the assessment of zooplankton grazing on bacteria, protozoans and microalgae, Freshwater Biol., 1997b, vol. 38, no. 3, pp. 629–637. https://doi.org/10.1046/j.1365-2427.1997.00241.x
Desvilettes, C., Bourdier, G., and Breton, J.C., On the occurrence of a possible bioconversion of linolenic acid into docosahexaenoic acid by the copepod Eucyclops serrulatus fed on microalgae, J. Plankton Res., 1997a, vol. 19, no. 2, pp. 273–278. https://doi.org/10.1093/plankt/19.2.273
Dijkman, N.A. and Kromkamp, J.C., Phospholipid-derived fatty acids as chemotaxonomic markers for phytoplankton: application for inferring phytoplankton composition, Mar. Ecol.: Prog. Ser., 2006, vol. 324, pp. 113–125. https://doi.org/10.3354/meps324113
Downing, J.A., Plante, C., and Lalonde, S., Fish production correlated with primary productivity, not the morphoedaphic Index, Can. J. Fish. Aquat. Sci., 1990, vol. 47, no. 8, pp. 1929–1936. https://doi.org/10.1139/f90-217
Dubovskaya, O.P., Non-predatory mortality of the crustacean zooplankton, and its possible causes (a review), Zh. Obshch. Biol., 2009, vol. 70, no. 2, pp. 168–192.
Edwards, K.F., Klausmeier, C.A., and Litchman, E., Evidence for a three-way trade-off between nitrogen and phosphorus competitive abilities and cell size in phytoplankton, Ecology, 2011, vol. 92, no. 11, pp. 2085–2095. https://doi.org/10.1890/11-0395.1
Eixler, S., Karsten, U., and Selig, U., Phosphorus storage in Chlorella vulgaris (Trebouxiophyceae, Chlorophyta) cells and its dependence on phosphate supply, Phycologia, 2006, vol. 45, no. 1, pp. 53–60. https://doi.org/10.2216/04-79.1
Elser, J.J., Dobberfuhl, D.R., MacKay, N.A., and Schampel, J.H., Organism size, life history, and N:P stoichiometry: Toward a unified view of cellular and ecosystem processes, Bioscience, 1996, vol. 46, no. 9, pp. 674–684. https://doi.org/10.2307/1312897
Elser, J.J., O’Brien, W.J., Dobberfuhl, D.R., and Dowling, T.E., The evolution of ecosystem processes: growth rate and elemental stoichiometry of a key herbivore in temperate and arctic habitats, J. Evol. Biol., 2000, vol. 13, pp. 845–853.
Feniova, I.Yu., Sakharova, E.G., Gladyshev,M.I., Sushchik, N.N., Gorelysheva, Z.I., and Karpowicz, M., Effects of fish on the transfer efficiency of carbon, PUFA and nutrients from phytoplankton to zooplankton under eutrophic conditions, Biol. Bull., 2021, vol. 48, no. 8, pp. 1284–1297. https://doi.org/10.1134/S1062359021080070
Feniova, I., Dawidowicz, P., Ejsmont-Karabin, J., Gladyshev, M., Kalinowska, K., Karpowicz, M., Kostrzewska-Szlakowska, I., Majsak, N., Petrosyan, V., Razlutskij, V., Rzepecki, M., Sushchik, N., and Dzialowski, A.R., Effects of zebra mussels on cladoceran communities under eutrophic conditions, Hydrobiologia, 2018, vol. 822, pp. 37–54. https://doi.org/10.1007/s10750-018-3699-4
Feniova, I., Dawidowicz, P., Gladyshev, M.I., Kostrzewska-Szlakowska, I., Rzepecki, M., Razlutskij, V., Sushchik, N.N., Majsak, N., and Dzialowski, A.R., Experimental effects of large-bodied Daphnia, fish and zebra mussels on cladoceran community and size structure, J. Plankton Res., 2015, vol. 37, no. 3, pp. 611–625. https://doi.org/10.1093/plankt/fbv022
Feniova, I., Sakharova, E., Karpowicz, M., Gladyshev, M.I., Sushchik, N.N., Dawidowicz, P., Gorelysheva, Z., Górniak, A., Stroinov, Y., and Dzialowski, A., Direct and indirect impacts of fish on crustacean zooplankton in experimental mesocosms, Water, 2019, vol. 11, art. ID 2090. https://doi.org/10.3390/w11102090
Feniova, I., Sakharova, E.G., Gorelysheva, Z.I., Karpowicz, M., Górniak, A., Petrosyan, V., and Dzialowski, A.R., Effects of zebra mussels (Dreissena polymorpha) on phytoplankton community structure under eutrophic conditions, Aquat. Invasions, 2020, vol. 15, no. 3, pp. 435–454. https://doi.org/10.3391/ai.2020.15.3.05
Feniova, I.Y., Karpowicz, M., Gladyshev, M.I., Sushchik, N.N., Petrosyan, V.G., Sakharova, E.G., and Dzialowski, A.R., Effects of macrobiota on the transfer efficiency of essential elements and fatty acids from phytoplankton to zooplankton under eutrophic conditions, Front. Environ. Sci., 2021, vol. 9, art. ID 739014. https://doi.org/10.3389/fenvs.2021.739014
Finkel, Z.V., Beardall, J., Flynn, K.J., Quigg, A., Rees, T.A.V., and Raven, J.A., Phytoplankton in a changing world: cell size and elemental stoichiometry, J. Plankton Res., 2010, vol. 32, no. 1, pp. 119–137. https://doi.org/10.1093/plankt/fbp098
Frost, P.C., Evans-White, M.A., Finkel, Z.V., Jensen, T.C., and Matzek, V., Are you what you eat? Physiological constraints on organismal stoichiometry in an elementally imbalanced world, Oikos, 2005, vol. 109, no. 1, pp. 18–28. https://doi.org/10.1111/j.0030-1299.2005.14049.x
Galloway, A.W.E. and Winder, M., Partitioning the relative importance of phylogeny and environmental conditions on phytoplankton fatty acids, PLoS One, 2015, vol. 10, no. 6 art. ID e0130053. https://doi.org/10.1371/journal.pone.0130053
Gladyshev, M.I., Essential polyunsaturated fatty acids and their dietary sources for man, Zh. Sib. Fed. Univ., 2012, vol. 5, no. 4, pp. 352–386.
Gladyshev, M.I., Sushchik, N.N., Anishchenko, O.V., Makhutova, O.N., Kolmakov, V.I., Kalachova, G.S., Kolmakova, A.A., and Dubovskaya, O.P., Efficiency of transfer of essential polyunsaturated fatty acids versus organic carbon from producers to consumers in a eutrophic reservoir, Oecologia, 2011, vol. 165, pp. 521–531. https://doi.org/10.1007/s00442-010-1843-6
Gladyshev, M.I., Sushchik, N.N., Dubovskaya, O.P., Buseva, Z.F., Makhutova, O.N., Fefilova, E.N., Feniova, I.Y., Semenchenko, V.P., Kolmakova, A.A., and Kalachova, G.S., Fatty acid composition of Cladocera and Copepoda from lakes of contrasting temperature, Freshwater Biol., 2015, vol. 60, no. 2, pp. 373–386. https://doi.org/10.1111/fwb.12499
Gladyshev, M.I., Sushchik, N.N., Kolmakova, A.A., Kalachova, G.S., Kravchuk, E.S., Ivanova, E.A., and Makhutova, O.N., Seasonal correlations of elemental and ω3 PUFA composition of seston and dominant phytoplankton species in a eutrophic Siberian Reservoir, Aquat. Ecol., 2007, vol. 41, pp. 9–23. https://doi.org/10.1007/s10452-006-9040-8
Gladyshev, M.I., Temerova, T.A., Dubovskaya, O.P., Kolmakov, V.I., and Ivanova, E.A., Selective grazing on Cryptomonas by Ceriodaphnia quadrangula fed a natural phytoplankton assemblage, Aquat. Ecol., 1999, vol. 33, pp. 347–353.
Gliwicz, Z.M., Between hazards of starvation and risk of predation: the ecology of off-shore animals, Excellence in Ecology, Germany: Oldendorf/Luhe, 2003.
Gugger, M., Lyra, C., Suominen, I., Tsitko, I., Humbert, J.-F., Salkinoja-Salonen, M.S., and Sivonen, K., Cellular fatty acids as chemotaxonomic markers of the genera Anabaena, Aphanizomenon, Microcystis, Nostoc and Planktothrix (cyanobacteria), Int. J. Syst. Evol. Microbiol., 2002, vol. 52, no. 3, pp. 1007–1015. https://doi.org/10.1099/00207713-52-3-1007
Guschina, I.A. and Harwood, J.L., Mechanisms of temperature adaptation in poikilotherms, FEBS Lett., 2006, vol. 580, no. 23, pp. 5477–5483. https://doi.org/10.1016/j.febslet.2006.06.066
Gutseit, K., Berglund, O., and Granéli, W., Essential fatty acids and phosphorus in seston from lakes with contrasting terrestrial dissolved organic carbon content, Freshwater Biol., 2007, vol. 52, no. 1, pp. 28–38. https://doi.org/10.1111/j.1365-2427.2006.01668.x
Happey-Wood, C.M. and Pentecost, A., Algal bioassay of the water from two linked but contrasting Welsh lakes, Freshwater Biol., 1981, vol. 11, no. 5, pp. 473–491. https://doi.org/10.1111/j.1365-2427.1981.tb01278.x
Heckmann, L.-H., Sibly, R.M., Timmermans, M.JTN., and Callaghan, A., Outlining eicosanoid biosynthesis in the crustacean Daphnia, Front. Zool., 2008, vol. 5, art. ID 11. https://doi.org/10.1186/1742-9994-5-11
Hessen, D.O. and Leu, E., Trophic transfer and trophic modification of fatty acids in high Arctic lakes, Freshwater Biol., 2006, vol. 51, no. 11, pp. 1987–1998. https://doi.org/10.1111/j.1365-2427.2006.01619.x
Hessen, D.O., Carbon, nitrogen and phosphorus status in Daphnia at varying food conditions, J. Plankton Res., 1990, vol. 12, no. 6, pp. 1239–1249. https://doi.org/10.1093/plankt/12.6.1239
Hessen, D.O., Elser, J.J., Sterner, R.W., Urabe J. Ecological stoichiometry: an elementary approach using basic principles, Limnol. Oceanogr., 2013, vol. 58, no. 6, pp. 2219–2236. https://doi.org/10.4319/lo.2013.58.6.2219
Hessen, D.O., Nutrient element limitation of zooplankton production, Am. Nat., 1992, vol. 140, no. 5, pp. 799–814.
Hixson, S.M. and Arts, M.T., Climate warming is predicted to reduce omega-3, long-chain, polyunsaturated fatty acid production in phytoplankton, Global Change Biol., 2016, vol. 22, no. 8, pp. 2744–2755. https://doi.org/10.1111/gcb.13295
Iwabuchi, T. and Urabe, J., Phosphorus acquisition and competitive abilities of two herbivorous zooplankton, Daphnia pulex and Ceriodaphnia quadrangular, Ecol. Res., 2010, vol. 25, no. 3, pp. 619–627.
Izquierdo, M.S., Fernandez-Palacios, H., and Tacon, A.G.J., Effect of broodstock nutrition on reproductive performance of fish, Aquaculture, 2001, vol. 197, no. 1–4, pp. 25–42. https://doi.org/10.1016/S0044-8486(01)00581-6
Jardine, T.D., Galloway, A.W.E., and Kainz, M.J., U-nlocking the power of fatty acids as dietary tracers and metabolic signals in fishes and aquatic invertebrates, Philos. Trans. R. Soc., 2020, vol. 375, no. 1804, art. ID 20190639. https://doi.org/10.1098/rstb.2019.0639
Kainz, M., Arts, M.T., and Mazumder, A., Essential fatty acids in the planktonic food web and their ecological role for higher trophic levels, Limnol. Oceanogr., 2004, vol. 49, no. 5, pp. 1784–1793. https://doi.org/10.4319/lo.2004.49.5.1784
Karpowicz, M., Feniova, I., Gladyshev, M.I., Ejsmont-Karabin, J., Górniak, A., Zieliński, P., Dawidowicz, P., Kolmakova, A.A., and Dzialowski, A.R., The stoichiometric ratios (C:N:P) in a pelagic food web under experimental conditions, Limnologica, 2019, vol. 77, art. ID 125690. https://doi.org/10.1016/j.limno.2019.125690
Kelly, J.R. and Scheibling, R.E., Fatty acids as dietary tracers in benthic food webs, Mar. Ecol.: Prog. Ser., 2012, vol. 446, pp. 1–22. https://doi.org/10.3354/meps09559
Klausmeier, C.A., Litchman, E., Daufresne, T., and Levin, S.A., Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton, Nature, 2004, vol. 429, no. 6988, pp. 171–174.
Knoll, L.B., Sarnelle, O., Hamilton, S.K., Kissman, C.E.H., Wilson, A.E., Rose, J.B., and Morgan, M.R., Invasive zebra mussels (Dreissena polymorpha) increase cyanobacterial toxin concentrations in low-nutrient lakes, Can. J. Fish Aquat. Sci., 2008, vol. 65, pp. 448–455. https://doi.org/10.1139/f07-181
Kormilets, O.N., Fatty acids in food webs of inland water ecosystems, Doctoral (Biol.) Dissertation, Krasnoyarsk, 2019.
Lacroix, G., Lescher-Moutoue, F., and Bertolo, A., Biomass and production of plankton in shallow and deep lakes: are there general patterns?, Ann. Limnol., 1999, vol. 35, no. 2, pp. 111–122. https://doi.org/10.1051/limn/1999016
Leonard, A.E., Pereira, S.L., Sprecher, H., and Huang, Y-S., Elongation of long-chain fatty acids, Prog. Lipid Res., 2004, vol. 43, pp. 36–54. https://doi.org/10.1016/s0163-7827(03)00040-7
Levich, A.P. and Bulgakov, N.G., Regulation of species and size composition in phytoplankton communities in situ by N:P ratio, Russ. J. Aquat. Ecol., 1992, vol. 2, pp. 149–159.
Lin, C.K. and Schelske, C.L., Seasonal variation of potential nutrient limitation to chlorophyll production in southern Lake Huron, Can. J. Fish Aquat. Sci., 1981, vol. 38, pp. 1–9. https://doi.org/10.1139/f81-001
Lindeman, R.L., The trophic–dynamic aspect of ecology, Ecology, 1942, vol. 23, no. 4, pp. 399–418.
Loladze, I. and Elser, J.J., The origins of the Redfield nitrogen-to-phosphorus ratio are in a homoeostatic protein-to-rRNA ratio, Ecol. Lett., 2011, vol. 14, no. 3, pp. 244–250. https://doi.org/10.1111/j.1461-0248.2010.01577.x
Makhutova, O.N., Protasov, A.A., Gladyshev, M., Sylaieva, A.A., Sushchik, N.N., Morozovskaya, I.A, and Kalachova, G.S., Feeding spectra of bivalve mollusks Unio and Dreissena from Kanevskoe Reservoir, Ukraine: are they food competitors or not?, Zool. Stud., 2013, vol. 52, no. 56, art. ID 56.
Martin-Creuzburg, D., Wacker, A., and Basena, T., Interactions between limiting nutrients: Consequences for somatic and population growth of Daphnia magna, Limnol. Oceanogr., 2010, vol. 55, no. 6, pp. 2597–2607. https://doi.org/10.4319/lo.2010.55.6.2597
Müller-Navarra, D.C., Brett, M.T., Liston, A.M., and Goldman, C.R., A highly unsaturated fatty acid predicts carbon transfer between primary producers and consumers, Nature, 2000, vol. 403, pp. 74–77.
Müller-Navarra, D.C., Brett, M.T., Park, S., Chandra, S., Ballantyne, A.P., Zorita, E., and Goldman, C.R., Unsaturated fatty acid content in seston and tropho-dynamic coupling in lakes, Nature, 2004, vol. 427, pp. 69–72.
Okun, N. and Mehner, T., Distribution and feeding of juvenile fish on invertebrates in littoral reed (Phragmites) stands, Ecol. Freshwater Fish, 2005, vol. 14, no. 2, pp. 139–149. https://doi.org/10.1111/j.1600-0633.2005.00087.x
Olsen, Y., Jensen, A., Reinertsen, H., Børsheim, K.Y., Heldal, M., and Langeland, A., Dependence of the rate of release of phosphorus by zooplankton on the P:C ratio in the food supply, as calculated by a recycling model, Limnol. Oceanogr., 1986, vol. 31, no. 1, pp. 34–44. https://doi.org/10.4319/lo.1986.31.1.0034
Parrish, C.C., Whiticar, M., and Puvanendran, V., Is ω6 docosapentaenoic acid an essential fatty acid during early ontogeny in marine fauna?, Limnol. Oceanogr., 2007, vol. 52, no. 1, pp. 476–479. https://doi.org/10.4319/lo.2007.52.1.0476
Persson, J., Brett, M.T., Vrede, T., and Ravet, J.L., Food quantity and quality regulation of trophic transfer between primary producers and a keystone grazer (Daphnia) in pelagic freshwater food webs, Oikos, 2007, vol. 116, no. 7, pp. 1152–1163. https://doi.org/10.1111/j.0030-1299.2007.15639.x
Powell, N., Shilton, A., Chisti, Y., and Pratt, S., Towards a luxury uptake process via microalgae—Defining the polyphosphate dynamics, Water Res., 2009, vol. 43, no. 17, pp. 4207–4213. https://doi.org/10.1016/j.watres.2009.06.011
Prater, C., Wagner, N.D., and Frost, P.C., Seasonal effects of food quality and temperature on body stoichiometry, biochemistry, and biomass production in Daphnia populations, Limnol. Oceanogr., 2018, vol. 63, no. 4, pp. 1727–1740. https://doi.org/10.1002/lno.10803
Raikow, D.F., Sarnelle, O., Wilson, A.E., and Hamilton, S.K., Dominance of the noxious cyanobacterium Microcystis aeruginosa in low-nutrient lakes is associated with exotic zebra mussels, Limnol. Oceanogr., 2004, vol. 49, no. 2, pp. 482–487. https://doi.org/10.4319/lo.2004.49.2.0482
Ravet, J.L., Brett, M.T., and Arhonditsis, G.B., The effects of seston lipids on zooplankton fatty acid composition in Lake Washington, Washington, USA, Ecology, 2010, vol. 91, no. 1, pp. 180–190. https://doi.org/10.1890/08-2037.1
Redfield, A.C., On the proportions of organic derivatives in sea water and their relation to the composition of plankton, James Johnstone Memorial Volume, Liverpool: University Press of Liverpool, 1934, pp. 176–192.
Reynolds, C., Ecology of Phytoplankton, Cambridge: Cambridge University Press, 2006.
Sakharova, E.G., Karpowicz, M., Gladyshev, M.I., Sushchik, N.N., Gorelysheva, Z.I., and Feniova, I.Yu., Effects of Dreissena polymorpha on the transfer efficiency of carbon, fatty acids, nitrogen, and phosphorus from phytoplankton to zooplankton, Zh. Obshch. Biol., 2021, vol. 82, no. 3, pp. 188–200. https://doi.org/10.31857/S0044459621030052
Sargent, J., Bell, G., McEvoy, L., Tocher, D., and Estevez, A., Recent developments in the essential fatty acid nutrition of fish, Aquaculture, 1999, vol. 177, nos. 1–4, pp. 191–199. https://doi.org/10.1016/S0044-8486(99)00083-6
Sarnelle, O., White, J.D., Horst, G.P., and Hamilton, S.K., Phosphorus addition reverses the positive effect of zebra mussels (Dreissena polymorpha) on the toxic cyanobacterium, Microcystis aeruginosa, Water Res., 2012, vol. 46, no. 11, pp. 3471–3478. https://doi.org/10.1016/j.watres.2012.03.050
Schmitz, G. and Ecker, J., The opposing effects of n-3 and n-6 fatty acids, Prog. Lipid Res., 2008. vol. 47, no. 2, pp. 147–155. https://doi.org/10.1016/j.plipres.2007.12.004
Schulhof, M.A., Shurin, J.B., and Declerck, S.A.J., Van de Waal D.B. Phytoplankton growth and stoichiometric responses to warming, nutrient addition and grazing depend on lake productivity and cell size, Global Change Biol., 2019, vol. 25, no. 8, pp. 2751–2762. https://doi.org/10.1111/gcb.14660
Sommer, U. and Sommer, F., Cladocerans versus copepods: the cause of contrasting top–down controls on freshwater and marine phytoplankton, Oecologia, 2006, vol. 147, pp. 183–194.
Sperfeld, E. and Wacker, A., Temperature- and cholesterol induced changes in eicosapentaenoic acid limitation of Daphnia magna determined by a promising method to estimate growth saturation thresholds, Limnol. Oceanogr., 2011, vol. 56, no. 4, pp. 1273–1284. https://doi.org/10.4319/lo.2011.56.4.1273
Sterner, R.W. and Elser, J.J., Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere, Oxford: Princeton Univ. Press, 2002.
Sterner, R.W. and Hessen, D.O., Algal nutrient limitation and the nutrition of aquatic herbivores, Annu. Rev. Ecol. Syst., 1994, vol. 25, pp. 1–29. https://doi.org/10.1146/annurev.es.25.110194.000245
Sterner, R.W., Daphnia growth on varying quality of Scenedesmus: mineral limitation of zooplankton, Ecology, 1993, vol. 74, no. 8, pp. 2351–2360. https://doi.org/10.2307/1939587
Sterner, R.W., Modelling interactions of food quality and quantity in homeostatic consumers, Freshwater Biol., 1997, vol. 38, no. 3, pp. 473–481. https://doi.org/10.1046/j.1365-2427.1997.00234.x
Sterner, R.W., The ratio of nitrogen to phosphorus resupplied by herbivores: Zooplankton and the algal competitive arena, Am. Nat., 1990, vol. 136, no. 2, pp. 209–229.
Sterner, R.W., The role of grazers in phytoplankton succession, Plankton Ecology, Brock: Springer-Verlag, 1989, pp. 107–170.
Strandberg, U., Taipale, S.J., Hiltunen, M., Galloway, A.W.E., Brett, M.T., and Kankaala, P., Inferring phytoplankton community composition with a fatty acid mixing model, Ecosphere, 2015, vol. 6, no. 1, pp. 1–14. https://doi.org/10.1890/ES14-00382.1
Sushchik, N.N., Gladyshev, M.I., Makhutova, O.N., Kalachova, G.S., Kravchuk, E.S., and Ivanova, E.A., Associating particulate essential fatty acids of the ω3 family with phytoplankton species composition in a Siberian reservoir, Freshwater Biol., 2004, vol. 49, no. 9, pp. 1206–1219. https://doi.org/10.1111/j.1365-2427.2004.01263.x
Sushchik, N.N., Kalachova, G.S., Zhila, O.N., Gladyshev, M.I., and Volova, T.G., A temperature dependence of the intra- and extracellular fatty acid composition of green algae and cyanobacterium, Russ. J. Plant Physiol., 2003, vol. 50, pp. 374–380.
Taipale, S., Strandberg, U., Peltomaa, E., Galloway, A.W.E., Ojala, A., and Brett, M.T., Fatty acid composition as biomarkers of freshwater microalgae: analysis of 37 strains of microalgae in 22 genera and in seven classes, Aquat. Microb. Ecol., 2013, vol. 71, no. 2, pp. 165–178. https://doi.org/10.3354/ame01671
Taipale, S.J., Kainz, M.J., and Brett, M.T., Diet-switching experiments show rapid accumulation and preferential retention of highly unsaturated fatty acids in Daphnia, Oikos, 2011, vol. 120, no. 11, pp. 1674–1682. https://doi.org/10.1111/j.1600-0706.2011.19415.x
Taipale, S.J., Vuorio, K., Brett, M.T., Peltomaa, E., Hiltunen, M., and Kankaala, P., Lake zooplankton delta C-13 values are strongly correlated with the delta C-13 values of distinct phytoplankton taxa, Ecosphere, 2016, vol. 7, no. 8, art. ID e01392. https://doi.org/10.1002/ecs2.1392
Tocher, D.R., Leaver, M.J., and Hodson, P.A., Recent advances in the biochemistry and molecular biology of fatty acyl desaturase, Prog. Lipid Res., 1998, vol. 37, pp. 73–117. https://doi.org/10.1016/s0163-7827(98)00005-8
Toseland, A., Daines, S.J., Clark, J.R., Kirkham, A., Strauss, J., Uhlig, C., and Mock, T., The impact of temperature on marine phytoplankton resource allocation and metabolism, Nat. Clim. Change, 2013, vol. 3, no. 11, pp. 979–984.
Twining, C.W., Brenna, J.T., Hairston, N.G., and Flecker, A.S., Highly unsaturated fatty acids in nature: What we know and what we need to learn, Oikos, 2016, vol. 125, no. 6, pp. 749–760. https://doi.org/10.1111/oik.02910
Urabe, J. and Watanabe, Y., Possibility of N or P limitation for planktonic cladocerans: An experimental test, Limnol. Oceanogr., 1992, vol. 37, no. 2, pp. 244–251. https://doi.org/10.4319/lo.1992.37.2.0244
Vanderploeg, H.A., Sarnelle, O., Liebig, J.R., Morehead, N.R., Robinson, S.D., Johengen, T.H., and Horst, G.P., Seston quality drives feeding, stoichiometry and excretion of zebra mussels, Freshwater Biol., 2017, vol. 62, no. 4, pp. 664–680. https://doi.org/10.1111/fwb.12892
Vanni, M.J., Nutrient cycling by animals in freshwater ecosystems, Annu. Rev. Ecol. Syst., 2002, vol. 33, pp. 341–370. https://doi.org/10.1146/annurev.ecolsys.33.010802.150519
Velthuis, M., De Senerpont Domis, L.N., Frenken, T., Stephan, S., Kazanjian, G., Aben, R., Kosten, S., Van Donk, E., and Van De Waal, D.B., Warming advances top-down control and reduces producer biomass in a freshwater plankton community, Ecosphere, 2017, vol. 8, no. 1, pp. 1–16. https://doi.org/10.1002/ecs2.1651
Waajen, G.W.A.M., Van Bruggen, N.C.B., Pires, L.M.D., Lengkeek, W., and Lürling, M., Biomanipulation with quagga mussels (Dreissena rostriformis bugensis) to control harmful algal blooms in eutrophic urban ponds, Ecol. Eng., 2016, vol. 90, pp. 141–150. https://doi.org/10.1016/j.ecoleng.2016.01.036
Wagner, N.D., Hillebrand, H., Wacker, A., and Frost, P.C., Nutritional indicators and their uses in ecology, Ecol. Lett., 2013, vol. 16, no. 4, pp. 535–544. https://doi.org/10.1111/ele.12067
Wagner, N.D., Lankadurai, B.P., Simpson, M.J., Simpson, A.J., and Frost, P.C., Metabolomic differentiation of nutritional stress in an aquatic invertebrate, Physiol. Biochem. Zool., 2015, vol. 88, no. 1, pp. 43–52. https://doi.org/10.1086/679637
Weers, P.M.M., Siewertsen, K., and Gulati, R., Is the fatty acid composition of Daphnia galeata determined by the fatty acid composition of the ingested diet?, Freshwater Biol., 1997, vol. 38, no. 3, pp. 731–738. https://doi.org/10.1046/j.1365-2427.1997.00238.x
White, T.C.R., The Inadequate Environment: Nitrogen and the Abundance of Animals, Berlin: Springer-Verlag, 1993.
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The analysis and interpretation of the literature on zooplankton were supported by the Russian Science Foundation, project no. 21-14-00123, and the literature on phytoplankton was analyzed and interpreted as part of State Task topic no. 121051100099-5. The preparation of the manuscript by Feniova I. was supported by the Polish National Agency for Academic Exchange (Agreement No. PPN/ULM/2020/ 1/00258/U/DRAFT/00001).
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Feniova, I.Y., Sakharova, E.G. & Krylov, A.V. Transfer of Essential Substances from Phytoplankton to Zooplankton in Freshwater Ecosystems (Review). Contemp. Probl. Ecol. 15, 315–326 (2022). https://doi.org/10.1134/S1995425522040059
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DOI: https://doi.org/10.1134/S1995425522040059